15
Downloaded By: [Chonnam National University] At: 02:36 7 April 2008 Critical Reviews in Food Science and Nutrition, 46:749–763 (2007) Copyright C Taylor and Francis Group, LLC ISSN: 1040-8398 DOI: 10.1080/10408390601062211 Plant Stress Physiology: Opportunities and Challenges for the Food Industry FEDERICO G ´ OMEZ GALINDO and INGEGERD SJ ¨ OHOLM Department of Food Engineering, Lund University, P.O. Box 124, SE-221 00, Lund, Sweden ALLAN G. RASMUSSON and SUSANNE WIDELL Department of Cell and Organism Biology, Lund University, S¨ olvegatan 35B, SE-223 62 Lund, Sweden KARL KAACK Department of Food Science, Danish Institute of Agricultural Sciences, Kristinebjergvej 10, DK-5792, Aarslev, Denmark We review and analyze the possible advantages and disadvantages of plant-stress-related metabolic and structural changes on applications in the fruit and vegetable processing industry. Knowledge of the cellular and tissue transformations that result from environmental conditions or industrial manipulation is a powerful means for food engineers to gain a better understanding of biological systems in order to avoid potential side effects. Our aim is to provide an overview of the understanding and implementation of physiological and biochemical principles in the industrial processing of fruits and vegetables. Keywords stress tolerance, freezing, heat, drought, drying, postharvest, minimal processing INTRODUCTION Because plants are confined to the place in which they grow, they have a limited capacity to avoid unfavorable conditions in their environment, such as extremes of temperature, water shortage, insufficient or excessive light or mineral nutrients, wounding by herbivores, or attack by pathogenic bacteria, fungi, viruses, and viroids. Plants have developed sophisticated molec- ular chemical strategies to defend themselves against such abi- otic and biotic stress, often combined with changes in growth and development patterns (Boyer, 1982; Gaspar et al., 2002). Stress is usually defined as an external factor that exerts a dis- advantageous influence on the plant. This concept is closely associated with stress tolerance, which is the plant’s capacity to cope with unfavorable conditions (Taiz and Zeiger, 2002). In both natural and agricultural conditions, environmental fac- tors, such as air temperature, can become stressful in just a few minutes. Soil water content may take days to weeks, whereas other factors such as soil mineral deficiency, can take months Address Correspondence to Federico G ´ omez Galindo, Department of Food Engineering, Lund University, P.O. Box 124, SE-221 00, Lund, Sweden. Tel: +4646 222 9814; Fax: +4646 222 9846; E-mail: [email protected] to become stressful. Cellular responses to stress may include changes in cell cycle and division, cell membranes, cell wall architecture, and metabolism (e.g. accumulation of osmotically active substances). From a biological point of view, industrial treatment of plant tissue will mimic stress (Fig. 1) and therefore, knowledge of how the plant material will be affected in relation to time, the environment, and industrial manipulation is of fundamental im- portance for quality assurance and process optimization. We here focus our attention on reviewing and analyzing possible advantages and disadvantages of the stress responses of fruits and vegetables during industrial processing operations. Reports on attempts to implement physiological and biochemical prin- ciples in the industrial processing of fruit and vegetables are not common in the literature, but a few recent investigations, referred to in the following sections, have laid the foundation for a fascinating area of research and technological innovation. STRESS LEADING TO CELL DAMAGE During harvesting, transportation, washing, sorting, and packing, fruits and vegetables are subjected to mechanical stress 749

2007 plant stress physiology- opportunities and challenges for the food industry

Embed Size (px)

DESCRIPTION

 

Citation preview

Page 1: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

Critical Reviews in Food Science and Nutrition, 46:749–763 (2007)Copyright C©© Taylor and Francis Group, LLCISSN: 1040-8398DOI: 10.1080/10408390601062211

Plant Stress Physiology:Opportunities and Challenges for theFood Industry

FEDERICO GOMEZ GALINDO∗ and INGEGERD SJOHOLMDepartment of Food Engineering, Lund University, P.O. Box 124, SE-221 00, Lund, Sweden

ALLAN G. RASMUSSON and SUSANNE WIDELLDepartment of Cell and Organism Biology, Lund University, Solvegatan 35B, SE-223 62 Lund, Sweden

KARL KAACKDepartment of Food Science, Danish Institute of Agricultural Sciences, Kristinebjergvej 10, DK-5792, Aarslev, Denmark

We review and analyze the possible advantages and disadvantages of plant-stress-related metabolic and structural changeson applications in the fruit and vegetable processing industry. Knowledge of the cellular and tissue transformations thatresult from environmental conditions or industrial manipulation is a powerful means for food engineers to gain a betterunderstanding of biological systems in order to avoid potential side effects. Our aim is to provide an overview of theunderstanding and implementation of physiological and biochemical principles in the industrial processing of fruits andvegetables.

Keywords stress tolerance, freezing, heat, drought, drying, postharvest, minimal processing

INTRODUCTION

Because plants are confined to the place in which they grow,they have a limited capacity to avoid unfavorable conditionsin their environment, such as extremes of temperature, watershortage, insufficient or excessive light or mineral nutrients,wounding by herbivores, or attack by pathogenic bacteria, fungi,viruses, and viroids. Plants have developed sophisticated molec-ular chemical strategies to defend themselves against such abi-otic and biotic stress, often combined with changes in growthand development patterns (Boyer, 1982; Gaspar et al., 2002).Stress is usually defined as an external factor that exerts a dis-advantageous influence on the plant. This concept is closelyassociated with stress tolerance, which is the plant’s capacityto cope with unfavorable conditions (Taiz and Zeiger, 2002).In both natural and agricultural conditions, environmental fac-tors, such as air temperature, can become stressful in just a fewminutes. Soil water content may take days to weeks, whereasother factors such as soil mineral deficiency, can take months

∗Address Correspondence to Federico Gomez Galindo, Department of FoodEngineering, Lund University, P.O. Box 124, SE-221 00, Lund, Sweden. Tel:+4646 222 9814; Fax: +4646 222 9846; E-mail: [email protected]

to become stressful. Cellular responses to stress may includechanges in cell cycle and division, cell membranes, cell wallarchitecture, and metabolism (e.g. accumulation of osmoticallyactive substances).

From a biological point of view, industrial treatment of planttissue will mimic stress (Fig. 1) and therefore, knowledge ofhow the plant material will be affected in relation to time, theenvironment, and industrial manipulation is of fundamental im-portance for quality assurance and process optimization. Wehere focus our attention on reviewing and analyzing possibleadvantages and disadvantages of the stress responses of fruitsand vegetables during industrial processing operations. Reportson attempts to implement physiological and biochemical prin-ciples in the industrial processing of fruit and vegetables arenot common in the literature, but a few recent investigations,referred to in the following sections, have laid the foundationfor a fascinating area of research and technological innovation.

STRESS LEADING TO CELL DAMAGE

During harvesting, transportation, washing, sorting, andpacking, fruits and vegetables are subjected to mechanical stress

749

Page 2: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

750 F. G. GALINDO ET AL.

Figure 1 Schematic representation of the topics discussed in this review. Industrial treatment of plant tissue will mimic stress responses in nature, influencingthe quality of fresh and processed products.

that may lead to crushing of surface cell layers. When the freshproducts reach the processing line for producing, for example,ready-to-use salads, they are typically peeled, sliced, diced, orshredded before packaging. These operations cut through cellsand leave intact cells of previously internal tissues exposed.These postharvest and processing operations are traumatic forthe cells proximal to the damage site and induce a complex se-ries of molecular events aimed at repairing the damage causedto the tissue (Surjadinata and Cisneros-Zevallos, 2003).

Response to Postharvest Handling

Mechanical stress, imposed on plant cells by a variety of phys-ical stimuli during harvesting and handling of fresh horticulturalproducts, induces a wide range of cellular responses such as in-creased respiration rate, ethylene production, and higher suscep-tibility to pathogen attack (Charron and Cantliffe, 1995; Stanley,1991). In carrots, mechanical stress brings about a decrease inroot pressure potential and water potential during the initial stor-age period (Mempel and Geyer, 1999; Herppich et al., 1999).Furthermore, the production of ethylene and 6-methoxymellein(a bitter compound) increases, whereas the levels of several ter-penes associated with the characteristic aroma of carrots de-creases (Seljasen et al., 2001). The accelerated aging in cu-cumbers involves the induction of cell-wall-degrading enzymes,leading to tissue degeneration (Miller and Kelley, 1989).

Potatoes are particularly susceptible to mechanical stress.Physically stressed tuber tissue produces melanin-basedpigments, leading to the blue-black discoloration of subdermaltissues known agronomically as black-spot bruising (Johnsonet al., 2003).This is a serious agronomic problem manifested

during harvesting, handling and storage, leading to significantlevels of rejection of potato harvests (Potato Marketing Board,1994). The synthesis of melanin is thought to be a defencemechanism in which the polymerized, insoluble complexesform a resistant barrier, sealing tuber tissues against the entryand spread of pathogens. The predisposition of tubers to melaninproduction depends on growth and storage conditions andtemperature during processing, and exhibits a wide range of ge-netic variation (Hoffmann and Wormanns, 2002; Johnson et al.,2003). Therefore, mechanical stress during handling (caused,e.g. by falls and collisions) induces wound responses leading toundesirable physiological changes, further reducing quality andstorability.

In spite of the many detrimental consequences of posthar-vest mechanical stress on the quality of fruit and vegetables,some reports have shown that slight mechanical stress duringgrowth can improve the postharvest processability of lettuce,cauliflower, celery (Biddington and Dearman, 1985; Pontinenand Voipio, 1992), and baby leaf salad (Clarkson et al., 2003),when the stress is applied to the seedlings. Mechanical stressduring growth results in modified leaf architecture producingsmaller, more compact new leaves. After industrial unit oper-ations including washing, drying, and packing, baby leaves oflettuce and spinach showed an increase in shelf-life. This in-crease was associated with a reduction in the area of individualepidermal cells and modification of the biophysical propertiesof the cell wall (Clarkson et al., 2003). The mechanical stressmanipulation of the seedlings led to the development of newadapted leaves with stiffer cell walls, so that the leaves wouldhave greater protection against mechanical stress during pro-cessing; stress that may otherwise cause damage and browningof the leaves (Lopez-Galvez et al., 1996). Smaller cells have

Page 3: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 751

a larger relative cell wall volume and dry weight (Wurr et al.,1986; Clarkson et al., 2003).

Effects on Minimally Processed Plant Tissue

As a result of peeling, grating, or shredding, a relatively stableagricultural product with a shelf life of several weeks or monthswill change into one that deteriorates rapidly from a food qualityperspective. Minimally processed fruit and vegetables shouldhave storage lives of at least 4–7 days, but preferably longer, upto 21 days depending on the market (Ahvenainen, 1996; Barry-Ryan and O’Beirne, 1997). Deterioration is mostly the result ofmicrobial spoilage, wound healing, biochemical changes, andloss of nutritional quality.

The quality and shelf life of minimally processed fruit andvegetables are directly influenced by the extent of woundingand the size of the wounded surface caused by the processingoperation. For example, it has been demonstrated that carrotspeeled by abrasion or sliced with a blunt machine blade showhigher respiration rates, greater microbial contamination andmicrobial growth rates, higher pH values in the carrot tissue,higher rates of weight loss, and higher white tissue developmentthan those that had been hand peeled or sliced with razor blades(Barry-Ryan and O’Beirne, 1998; 2000).

The respiration rate of fresh vegetable slices is in most cases3 to 5 times that of the intact organ, but aging of the sliced tissueelicits additional increase. Thus, the respiration rate of an agedslice may be 25 times that of the intact organ (Laties, 1978).Wadso et al. (2004) found that the overall metabolic activityof diced carrot, rutabaga, and potato tissue rose linearly with anincrease in cut surface area per unit volume (intensity of wound-ing), being as much as 40% higher when the surface area wasdoubled. This increase in metabolic activity is the consequenceof a large number of biosynthetic events taking place duringwound healing (Laties, 1978).

The initial physiological steps following wounding and thegeneration of wound signals are not fully understood (Saltveit,2000). Products of lipid metabolism and lipid oxidation as wellas compounds such as ethylene and abscisic acid (ABA), arethought to be possible candidates for the wound signals in plantcells (Pena-Cortes and Willmitzer, 1995).

When plant tissues are wounded, the cells near the site of thewounding stress strengthen their cell walls by the secretion of ad-ditional structural components such as lignin or suberin, creatinga protective layer immediately below the site of damage, to pre-vent dehydration and potential penetration by pathogens (Satohet al.,1992; Kaack et al., 2002b). The synthesis of several se-creted proteins, such as hydroxyproline-rich glycoproteins, andtheir cross-linking to the cell wall after wounding has also beenobserved (Showalter and Varner, 1987; Bradley et al., 1992).

Suberization is a regulated process whereby the intercellularspaces in tissues become impregnated with a poly(phenolic) ma-trix concomitant with the deposition of a poly(aliphatic) matrixbetween the plasmalemma and carbohydrate cell wall (Fried-

man, 1997; Bernards et al., 1999). The oxidative coupling ofthe poly(phenolic) component of suberin is thought to be aperoxidase/H2O2-dependent, free-radical process. In responseto wounding, and in association with suberization, plant tis-sues generate reactive oxygen species (ROS), including super-oxide (O−

2 ), hydrogen peroxide (H2O2), and the hydroxyl radical(OH.). It has been shown that H2O2 is essential for suberizationin potato slices (Razem and Bernards, 2002). Immediately fol-lowing wounding, a rapid increase in oxygen uptake is followedby an initial burst of ROS (oxidative burst) (Bolwell et al., 1995).In wounded potatoes, this burst reaches a maximum within 30to 60 min and is followed by at least three other massive burstsat 42, 63, and 100 h post-wounding. These later bursts were as-sociated with wound healing and are probably involved in theoxidative cross-linking of suberin poly(phenols) (Razem andBernards, 2003). The initial deposition of suberin in potato re-quires approximately 18 h at 18◦C (Lulai and Corsini, 1998)and reaches a stage in which the suberized layer has sufficientstructural integrity to be peeled off intact 3 days after wounding(Razem and Bernards, 2002).

Deposition of suberin may cause detrimental quality charac-teristics. For example, in the production of pre-peeled potatoes,a common industrial product in Scandinavia, hardening of thetuber surface takes place (Fig. 2a) (Kaack et al., 2002b). Thesepotatoes are too hard for consumption, even after cooking at 98–100◦C for one hour. Microscopic examination shows that whenhard potatoes are cooked, brick-like cells at the potato surfaceremain intact (Fig. 2b). It was demonstrated that potato harden-ing was significantly correlated to the mechanical impact of thepeeler, and was increased by blows during sorting or transport(Kaack et al. 2002a). However, the hardening of potato tissuedoes not occur if the tubers are steamed or cooked immediatelyor a few hours after peeling, probably because the exposed in-tact cells are killed. Therefore, understanding the dynamics andtime scales of the metabolic processes taking place in vegeta-bles during industrial unit operations is of great importance inprocessing design and optimization.

LOW-TEMPERATURE STRESS

Among the various kinds of environmental stress affectingplants, low temperature is of particular interest to food science,since low temperature, either chilling or freezing, is one of themost widespread and effective methods of conservation.

Low-Temperature Sweetening

Physiology

During the storage of some plant tissues at temperatures lowerthan those for optimum growth or storage (i.e.,<9–10◦C forpotatoes), the inverse hydrolysis of polysaccharides to disac-charides, and finally to monosaccharides takes place. This usu-ally occurs early during the storage period (Rutherford, 1981;Blenkinsop et al., 2004).

Page 4: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

752 F. G. GALINDO ET AL.

Figure 2 Microstructure of the surface of wounded potato tissue. (a) Raw surface with thick suberized (s) and curly cell walls (w). (b) Surface of cooked potatoshowing a few brick-like cells at (u) and gelatinized starch (G) with small regions of suberin.

In parsnip roots and potato tubers the increase in levels ofsucrose and other hexoses during low-temperature storage isknown as “cold sweetening” (Hart et al., 1986; Shattuck et al.,1989; Wismer et al., 1995; Espen et al., 1999). The cold-inducedincrease in soluble sugars may play a role in osmoregulation,cryoprotection (Espen et al., 1999) and possibly also in theactivation of respiratory metabolism. The genetic control andthe metabolic pathways of sugar synthesis have been studied(Deiting et al., 1998). In potatoes, the mechanism of cold sweet-ening is complex and is mediated by many interrelated metabolicpathways, such as the induction of the enzymes required instarch degradation, alterations in the biochemical pathways ofsucrose metabolism, glycolysis and mitochondrial respiration,as well as electrolyte leakage and membrane lipid peroxidation(Blenkinsop et al., 2004).

Implications for the Potato Crisp Industry

Blenkinsop et al. (2004) underlined the importance of the un-derstanding of metabolic changes in potatoes during cold storageto ensure satisfactory chip color in the potato chip industry. Colorcontrol is complicated as the color is determined by the chemicalcomposition of the tubers, which not only varies with season andcultivar, but changes during storage. Sugar levels and free aminoacids are important in determining the chip color, which is at-tributed to the products of the Maillard reaction. In addition to thecomplex carbohydrate metabolism, storage conditions and thelength of storage are also known to increase the free amino acidcontent and the amount of reducing sugars (Brierley et al., 1996).

In April 2002, the National Food Administration of Swedenand the University of Stockholm announced the presence of

Page 5: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 753

acrylamide, a possible carcinogenic, in foods processed athigh temperatures (Rosen and Hellenas, 2002; Tareke et al.,2002). As a result of high-temperature frying, potato-basedfood products, such as potato crisps, contain higher levels ofacrylamide than other baked or fried products (Chuda et al.,2003). Changes in the levels of reducing sugars and amino acidsin potato tubers during storage were investigated in relation tothe presence of acrylamide in the crisps. Chuda et al. (2003)found that crisps made from tubers stored at 2◦C contained tentimes more acrylamide than those made from tubers stored at20◦C. In the crisps, the acrylamide level did not depend on thelevels of total amino acids or aspargine, but on the availabilityof reducing sugars in the raw potato.

Generally, the tubers used to manufacture potato crisps arenot stored at such low temperatures as 2◦C, as they will producedark-colored crisps that are unacceptable to the consumer dueto their appearance and bitter taste (Roe et al., 1990). Therefore,potatoes are generally stored at around 10◦C in order to main-tain low levels of sugars during long-term storage (Blenkinsopet al., 2004). However, at this storage temperature potatoes willsprout, and the application of chemicals to inhibit sprouting maybe necessary. According to Blenkinsop et al. (2004), there hasbeen great interest during recent years in developing potato culti-vars (through traditional breeding and selection methods and/orthrough the use of genetic engineering) that are more resistantto low-temperature sweetening, and which have an acceptablecolor when processed directly after low-temperature storage(e.g. 4◦C), thus avoiding the application of sprout inhibitors.As stated above, levels of formation of acrylamide during fryingshould be another criterion for the development of such cultivars.

Chilling Injury

During growth and postharvest handling, chilling injury, de-fined as damage to susceptible plant species during exposureto low temperatures above the freezing point, leads to losses inyield and growth potential of crop plants and to reduced qualityof detached, edible tissues (Purvis and Shewfelt, 1993). Fruits ofmany species, especially those of tropical and subtropical originsuffer chilling injury upon exposure to non-freezing tempera-tures below 12◦C (Lafuente et al., 1991; Jaitrong et al., 2004).

Causes of Tissue Damage

A common response of sensitive plant cells to low tem-peratures is the disruption of membrane integrity (Purvis andShewfelt, 1993). In chilling-sensitive plants, the lipids in thebilayer have a high percentage of saturated fatty acid chains,and membranes with this composition tend to solidify into asemi-crystalline state at a temperature well above 0◦C (Parkinet al., 1989). Low temperature also affects membrane proteinsand enzymes. Protein-protein and protein-lipid interactions maybe weakened by a decrease in the relative strength of hydropho-bic bonding, leading to subunit dissociation and/or polypeptideunfolding (Stanley, 1991).

It has been shown that some of the effects of low-temperaturestress are mediated by reactive oxygen species (Aroca et al.,2003). The production of ROS is a phenomenon common tochilling and other stress conditions (e.g., cell damage), as indi-cated in the previous section. Under prolonged oxidative stressconditions, ROS cause lipid peroxidation, DNA damage, andprotein oxidative inactivation (Prasad, 1996). The activities ofcertain enzymes involved in keeping ROS at low levels, in-cluding superoxide dismutase and catalase, decrease. The con-sequence of this is a reduction in defence against free radi-cals and repair mechanisms. During exposure to stress the bal-ance between degradation and repair will be shifted towardsgreater degradation of susceptible tissues (Purvis and Shewfelt,1993).

Minimizing Chilling Injury After Harvest

Species that are sensitive to chilling can show appreciablevariation in their response to low temperatures. Also, tem-peratures that are considered “cold” vary between species(e.g. pineapple and carrot). Resistance to chilling injury oftenincreases if plants are first hardened (acclimated) by exposure tocool but non-injurious temperatures. Chilling damage thus canbe minimized if exposure is slow and gradual. Membrane lipidsfrom chilling-resistant plants often have a greater proportion ofunsaturated fatty acids than those from chilling-sensitive plants,and during acclimation to low temperatures the activity of lipiddesaturase enzymes increases and the proportion of unsaturatedlipids rises (Stanley, 1991; Palta et al., 1993). This modificationlowers the temperature at which the membrane lipids begina gradual phase change from fluid to semi-crystalline, andallows membranes to remain fluid at lower temperatures(Vandenbussche et al., 1999). For example, Marangoni et al.(1990) stored mature green commercial tomatoes at 12◦C for 4d followed by storage at 8◦C for 4 d, and then chilling at 5◦Cfor 15 d. The properties of these tomatoes were compared withthose directly chilled for 15 d at 5◦C. The gradual acclimationprogram decreased the severity of chilling injury, as reflectedin a more intense red color and a harder fruit, compared withwhat was observed in directly chilled tomatoes. Graduallycold-treated tomatoes showed an increase in the proportionof unsaturated fatty acids in their membranes, indicating thatacclimation had taken place. The described chilling responsewill also prepare plant tissues for potential freezing.

A direct response to chilling is a decrease in cellular res-piration. However, in many species acclimation results in therestoration of respiration (Atkin and Tjoelker, 2003), which maylead to increased respiratory losses during storage. Therefore,it is important to use procedures for thermal acclimation thatavoid respiratory reactivation.

Other methods of reducing or avoiding chilling injury havebeen described in the literature. They are based on the physio-logical response to another stress that protects the tissue againstchilling injury (cross-tolerance). These procedures will be de-scribed in more detail in following sections.

Page 6: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

754 F. G. GALINDO ET AL.

Freezing Injury

Freezing injury occurs at temperatures below the freezingpoint of water. Several plants, however, are able to inducetolerance to freezing, following a period of acclimation at cold,but non-freezing, temperatures (Smallwood and Bowles, 2002).

Physiology

The primary manifestation of cell damage by freezing is ob-served in the plasma membrane (Steponkus, 1984; Palta, 1990).The water potential of ice is lower than that of liquid water. Ex-tracellular ice crystals grow by drawing water from cells, thusdehydrating them, until the water potential of the ice and that ofwater in the cell are equal. The water potential of ice decreases asthe temperature decreases, so the extent of cellular dehydrationincreases with decreasing temperature, to a limit set by vitrifica-tion (glassy state) (Pearce, 2001). This deterioration is observedas wilting or softening of plant parts.

Plants that survive winter either prevent the crystallizationof ice within their tissues (freeze avoidance) or can withstandice crystallization in the apoplast (freeze tolerance) (Smallwoodand Bowles, 2002). Freeze avoidance involves supercooling andhence prevention of the incursion of ice into the apoplast. With-out ice nucleation, pure water can be supercooled to a certainpoint below 0◦C. However, this supercooling is only a practicalstrategy at the whole plant level when exposure to subzero tem-peratures is relatively brief (George et al., 1982; Smallwood andBowles, 2002). Some specialized cell types and organs use su-percooling as a strategy to overwinter, such as the xylem rayparenchyma cells of many trees, which supercool to around-40◦C (George and Burke, 1977). Given the widespread pres-ence of nucleators in the environment, the most common frostsurvival strategy is cold acclimation (freeze tolerance) and this isachieved through several changes in cell biochemistry regulatedat the gene expression level (Danyluk et al., 1998).

The accumulation of osmotically active substances, such assimple sugars, organic acids, proline, and glycinebetaine, is aprotective mechanism induced by cold stress (as previously de-scribed for cold sweetening). In many plants, sugars act as cry-oprotectants which increase the freezing resistance through di-rect and/or indirect effects (Graham and Patterson, 1982; Changand Reed, 2000). The hydrophilic nature of sugars is well-suitedto replace water and stabilize the cell membrane through hydro-gen bonding between hydroxyl groups on the sugar and po-lar residues in phospholipids, preventing dehydration effects inmembranes (Danyluk et al., 1998). Accumulation of osmoticallyactive substances leads to a decrease in the chemical potential ofwater. It has been suggested that this mechanism is involved inregulating the induction of cold-induced gene expression (Fuet al., 2000) and in the higher resistance of cold-acclimatedplants to fungal infection (Tronsmo, 1986).

Many cold-induced proteins accumulate in the tissues duringcold acclimation (reviewed by Thomashow, 1999). These canaccount for up to 0.9% of the total soluble proteins in winter

wheat after 21 days’ of cold acclimation (Houde et al., 1995),and have been found to be accumulated in many organelles,including the endoplasmic reticulum (Ukaji et al., 2001) andmitochondria (Zykova et al., 2002). The functions of theseproteins are not fully understood and have been the subject ofintense research during recent years. It has been speculated thatthey could have a detergent-like activity, coating hydrophobicsurfaces and thus preventing the coagulation of macromolecules(Smallwood and Bowles, 2002). Examples of proteins thataccumulate with cold acclimation include the cryoprotectiveproteins of spinach, rye, and other cereal antifreeze proteins(AFPs) (Thomashow, 1999). A factor common to all theseproteins is that they are predominantly located in the apoplastand are therefore more likely to come into contact with theouter surface of the plasma membrane.

AFPs are expressed in a number of plant species, such aswinter rye, winter barley, winter canola, white oak, and carrots,in response to low temperature (Urrutia et al., 1992; Duman andOlsen, 1993; Feeney and Yeh, 1993; Griffith and Antikainen,1996; Smallwood et al., 1999). Their accumulation and activityhave been found to be strongly correlated with winter survivaland it has been suggested that they be used as a biological markerfor crop improvement (Griffith et al., 1992; Chun et al., 1998).

Antifreeze proteins interact with ice crystals by adsorptiononto non-basal planes of ice at the ice-water interface thus mod-ifying their growth. At high AFP concentrations (µM), mini-mal crystal growth occurs, forming very small, stable hexago-nal bipyramids. Physical damage caused by ice can occur duringwarming, as well as during freezing, by a process known as re-crystallization (Knight and Duman, 1986; Breton et al., 2000).

Recrystallization of ice occurs when small ice crystals con-dense into larger ones. This can happen very quickly at tem-peratures just below the melting point of a frozen solution. Innature, prolonged exposure to subzero temperatures and tem-perature fluctuations may promote recrystallization of frozentissues, especially those in which cells are densely packed, andallow ice access to locations from which it is usually excluded.AFPs adsorbed onto the surfaces of ice act as potent inhibitors ofrecrystallization, even at very low concentrations (e.g. 1 µg/ml)(Worrall et al., 1998; Smallwood et al., 1999). Given that AFPsare also found in plant tissues where ice is allowed to crystal-lize in the apoplast (which includes the xylem, cell walls, andintercellular spaces), it has been speculated that inhibition of icerecrystallization may be the physiologically relevant aspect ofthe activity of AFPs (Smallwood and Bowles, 2002).

Application of Cold Acclimation in theFrozen-Vegetable Industry

When cold-stressed, starch-rich vegetables (e.g. potatoes)are frozen industrially, the effects of cold sweetening duringthe storage period could be detrimental to the quality of theproduct after cooking by the consumer at home (e.g., exces-sive brown color after frying, as discussed earlier). However,if vegetables accumulating mostly sucrose in their cytoplasm

Page 7: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 755

Figure 3 Conventional scanning electron micrographs showing the parenchyma of frozen carrots. Carrot slices from non-acclimated (a) and cold-acclimated (b)field-grown carrot taproots were covered with plastic film and frozen at −5◦C overnight. The samples were freeze-dried, fractured, and gold-sputtered. They wereexamined in a JEOL SEM 840-A microscope, operated at 15 kV and a working distance of 15 mm. The images show a remarkable contrast in the degree of tissuedamage caused by the freezing treatment between the acclimated and the non-acclimated carrots.

(e.g. carrots) and antifreeze proteins in their cell walls duringgrowth in the field in late autumn are to be frozen, industrymay take advantage of cold-induced stress responses to opti-mize the quality of the frozen product. The potential applicationof the acquisition of freezing tolerance by cold-acclimation ofcarrot taproots in the frozen-carrot industry has been discussed

by Gomez and Sjoholm (2004). The authors illustrated the en-hancement of the tolerance to freezing by the metabolic responseto low-temperature stress by freezing both acclimated and non-acclimated carrot slices at a very slow freezing rate (−5◦Cambient temperature over-night). Figure 3a shows a piece ofnon-acclimated carrot tissue that has been extensively damaged

Page 8: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

756 F. G. GALINDO ET AL.

by freezing. In remarkable contrast, Fig. 3b shows much moreintact tissue of the cold-acclimated samples frozen under thesame conditions. Although vegetables such as carrots are usuallyfrozen quickly to produce small ice crystals, these ice crystalsmay grow larger over time through recrystallization. Recrys-tallization occurs when temperature gradients form within theproduct during freezing or thawing, or when the temperaturefluctuates during storage or transportation (Griffith and Ewart,1995; Breton et al., 2000). Recrystallization in frozen foods canresult in membrane damage, thus reduced water holding capac-ity (high drip loss), and associated loss of nutrients (Fletcheret al., 1999; Breton et al., 2000). AFP is abundant in the accli-mated carrot tap root apoplast (0.5 mg of pure protein can beisolated from 1 kg of fully acclimated carrot taproots Smallwoodet al., 1999), and may be a key factor in inhibiting recrystalliza-tion and preserving the quality of the frozen product.

The potential benefits of cold acclimation of frozen carrotscan, however be eradicated by the common practice of blanchingbefore freezing. Heat will damage the cells, destroying the pro-tective system nature has created against frost damage. Aboveapproximately 50◦C, the functionality of the cell membrane isirreversibly damaged (De Belie et al., 2000). Denaturation ofproteins such as AFPs in the cell walls would also compromisethe cold acclimation effect, as these proteins must be foldedcorrectly in order to be active (M. Griffith, pers. comm.). Theoptimization of blanching to minimize tissue damage is thus veryimportant if the frozen-food industry is to be able to take advan-tage of cold acclimation to protect tissue cells (Gomez, 2004).

HEAT STRESS AND HEAT SHOCK

Most tissues of higher plants are unable to survive extendedexposure to high temperatures. Non-growing cells and dehy-drated tissue can tolerate much higher temperatures than hy-drated, growing cells. Actively growing tissues rarely survivetemperatures above 45◦C, but dry seeds can endure 120◦C andpollen grains of some species can remain viable after exposureto 70◦C (Taiz and Zeiger, 2002).

Storage of some legumes under tropical conditions (30–40◦C; >75% humidity) renders them susceptible to a hardeningphenomenon, causing nutritional losses and inflicting economiclosses on farmers and poor urban dwellers in developingcountries (Aguilera and Ballivian, 1987; Martin-Cabrejas andEsteban, 1995). This is an irreversible phenomenon knownas the hard-to-cook (HTC) defect. Beans with this defect arecharacterized by extended cooking times to achieve cotyledonsoftening, are less palatable to the consumer and are of lowernutritional value (Reyes-Moreno and Paredes-Lopez, 1993).

In many crops, as further discussed in this section, peri-odic, brief exposure to sublethal heat stress often induces tol-erance to otherwise lethal temperatures, a phenomenon knownas induced thermotolerance (Viswanathan and Khanna-Chopra,1996). Thermotolerance in crops is determined by a variety offactors such as photoperiod, light intensity and water availability(Ahn et al., 2004).

Causes of cell damage

Exposure of plants to temperatures above their optimalgrowth temperature can disrupt many essential metabolic pro-cesses, including photosynthesis and respiration, the former be-ing more sensitive. Activation of lipid peroxidation is one of theearliest and least stress-specific plasmalemmal responses causedby any stress agent, including heat shock. Lipid peroxidationcan result in various structural and functional disturbances inthe cell (Veselov et al., 2002). Furthermore, excessive fluidityof membrane lipids at high temperatures (above 50◦C) is cor-related with loss of functional cell compartmentalisation whichconsiderably enhances the permeability of membranes and, inconsequence, the passive flux of solutes (Kluge et al., 1991),leakage of electrolytes, and reduction of turgor pressure (DeBelie et al., 2000; Gonzalez-Martınez, 2003). It has been hypoth-esized that in beans susceptible to the HTC defect, the effects oftemperature on cell membrane are accompanied by lignificationof the cell wall, pectic de-esterification in the middle lamellaand breakdown of phytic acid, inhibiting chelation of divalentcations, which renders pectates in the middle lamella unsuscep-tible to softening during cooking (Aguilera and Ballivian, 1987,Reyes-Moreno and Paredes-Lopez, 1993).

High-temperature injury is also associated with lipid phasetransitions and/or changes in transmembrane protein conforma-tion (Hansen et al., 1994). Heat stress causes many cell proteins(enzymes or structural proteins) to become unfolded or mis-folded. Such misfolded proteins can aggregate and precipitate.

Plant Strategies for Heat Tolerance

Metabolic acclimation associated with heat tolerance mech-anisms includes an increase in the degree of saturation of fattyacids in membrane lipids, which makes the membranes less fluid,the synthesis of enzymes and isoenzymes with broad thermalkinetic windows, the synthesis of protective enzymes such asglutathione reductase, peroxidase, and catalase (Viswanathanand Khanna-Chopra, 1996), and the production of heat shockproteins (HSPs).

In response to sudden rises in temperature (5 to 10◦C), plantsproduce a unique set of proteins, the HSPs. Most HSPs func-tion as molecular chaperones, that is, they bind to unfolded ordenatured proteins, prevent aggregation and induce correct re-folding, facilitating correct cell function at elevated, stressfultemperatures. Some HSPs assist in polypeptide transport acrossmembranes into cellular compartments (Miroshnichenko et al.,2005).

Plants and most other organisms produce HSPs that havedifferent functions in response to increases in temperature:HSP100, HSP90, HSP70, HSP60, and small HSPs (smHSPs,15–30 kDa) (Vierling, 1991). HSP expression has been charac-terized in a variety of higher plants, including tomato (Banzet etal., 1998), maize (Cooper and Ho, 1983), soybean (Hsieh et al.,1992), carrot (Malik et al., 1999), pea (DeRocher et al., 1991),

Page 9: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 757

sugar cane (Hoisydai and Harrington, 1989), apple (Bowen et al.,2002), and potato (Ahn et al., 2004). Some smHSPs are knownto play an important role in the protection of biomembranes andorganelles (Viswanathan and Khanna-Chopra, 1996). Synthe-sizing a number of smHSPs at elevated temperatures is one ofthe unique features of the heat-shock response of plants (Ahnet al., 2004). Cells that have been induced to synthesize HSPsshow improved thermal tolerance and can withstand exposure totemperatures that are otherwise lethal (Malik et al., 1999; Bowenet al., 2002). It has been shown that a smHSP in tomato (VIS1)plays a role in facilitating fruit ripening, senescence, and seeddispersal by protecting the cellular machinery against thermaldenaturation during the daily cycles of daytime rise in tempera-ture. VIS1 acts as a chaperone by binding reversibly to enzymes,including cell wall polymer-modifying enzymes, and protectingthem from thermal denaturation (Ramakrishna et al., 2003).

In the food industry, heat treatment (generally 50–70◦C) hasbeen used for the past 40 years to improve the texture of veg-etables prior to high-temperature processing. The firming ef-fect of low-temperature blanching has been studied in a numberof vegetables (Bartolome et al., 1972; Lee et al., 1979; Stolle-Smits et al., 2000). Evidence indicates that the firming effectis due to the temperature activation of pectin methylesterase(PME, EC 3.1.1.11). The resulting reduction in the degree ofmethylesterification of the pectins in the cell wall and middlelamella allows the more calcium cross-linking between calciummolecules, increasing firmness (Pilnik and Voragen, 1991). Themechanism governing temperature activation of PME is notwell-understood. It has been speculated that, at elevated tem-peratures, a change in the PME enzyme or its environment mayoccur such that the enzyme is converted into a more active form.Loss of membrane integrity and leakage between cellular com-partments at temperatures >40◦C may contribute to this activa-tion (Anthon and Barrett, 2006). However, to our knowledge, noprevious study has associated PME activation with induction ofsignal cascades at the genetic level and/or metabolic transfor-mations strictly associated with the concept of “stress response”that we have been using throughout this review. It appears thatmild blanching treatment, for example, at 70◦C for 30 min (Leeet al., 1979), is used by the industry as a direct way of regulat-ing the activity of the enzyme. This treatment may mimic a truestress response that may occur at lower temperatures (around40◦C) for a longer time, for example, when harvested materiallies in the sun for hours before processing. A more detailed studyof the time and temperature dependence of PME activation andthe molecular mechanisms regulating it would be of interest.

Cross-Tolerance and its Application in Postharvest Handlingand Minimal Processing

In general, stress responses involve changes in the proteomeand metabolome with increased expression of proteins and com-patible solutes. Cross-talk between stress signalling pathwaysmay result in co-expression of stress responses (Joyce et al.,

2003). Thus, cells previously exposed to one kind of stress maygain protection against another kind (cross-tolerance). For exam-ple, some of the HSPs are not unique to high-temperature stressand can be induced by other forms of stress such as drought(Alamillo et al., 1995; Wehmeyer and Vierling, 2000), wound-ing, low temperature, and salinity (Wang et al., 2001). Symptomsof chilling injury are reduced after heat pretreatment, and thisreduction is correlated with persistence of several HSPs in fruittissue (Sabehat et al., 1996). Tomato and avocado fruits, in whichheat shock was induced (48 h at 38◦C), accumulated HSPs andwere protected from injury by subsequent chilling at 2◦C (Lurie,1998). Reduced chilling injury of cucumber cotyledons and cul-tured apple cells after exposure to 37 or 42◦C has also been re-ported (Lafuente et al., 1991; Wang et al., 2001). Heat treatmentat 38◦C for 8 h applied to evening-harvested sweet basil reducedits sensitivity to chilling. This reduction may have involved theantioxidative system of ROS protection, as suggested by theincreased reductive potential in the leaves, as well as the induc-tion of superoxide dismutase and catalase activity following heattreatment. Elevated activity remained through subsequent coldstorage below 12◦C (Faure-Mlynski et al., 2004).

Heat shock treatment has been used to reduce decay andchilling injury, and to enhance host resistance to pathogens infruits. Treatment by dipping in water at 52–53◦C for 2 min or62◦C for 20 s promoted the accumulation of HSPs and proline-rich proteins in the skin of grapefruit. Heat application has beenshown to markedly reduce decay and the sensitivity of citrus fruitto chilling injury without any deleterious effects on fruit quality(Ben-Yehoshua, 2003). Several types of machines for hot watertreatment are already in operation in many countries in packinghouses for citrus (Ben-Yehoshua, 2003) and other fruits, suchas bell peppers, corn cobs, lychees, mangos, melons, nectarines,and peaches (Fallik et al., 1999).

When cells are subjected to a stressful, but non-lethal tem-perature, the synthesis of HSPs increases dramatically, whilethe continuous translation of other proteins is lowered or ceases(Vierling, 1991). This effect has been seen in studies on thewounding stress response of carrots and lettuce. In the case ofcarrot slices, exposure to 40◦C for 1 h caused the cessation of thesynthesis and secretion of extensin proteins, a typical response towounding stress (Brodl and Ho, 1992). Maximum accumulationof HSPs was seen in the carrot slices one hour after a temperatureincrease from 28◦C to 40◦C. The synthesis of HSPs diminishedsharply after 3 h of continuous incubation at 40◦C and the carrotsresumed the secretion of extensin proteins during that period oftime. Upon recovery from 40◦C, the carrot slices resumed thesecretion of extensin and other cell wall proteins (Brodl and Ho,1992). This study demonstrates that high-temperature stress re-duces the response to wounding and nicely illustrates the factthat plant tissues follow a certain temporal order and hierarchyin their response to multiple stimuli. The heat-stressed, woundedtissue has basically redirected its resources towards the responseto more severe stress.

This principle has been applied in the minimal processing ofvegetables to prevent browning of wounded lettuce leaf tissue.

Page 10: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

758 F. G. GALINDO ET AL.

Wound-induced browning has been significantly reduced in ice-berg lettuce by the application of short thermal stress (Loaiza-Velarde et al., 1997). A heat shock of 45◦C for 90 s effectivelyprevents the synthesis of phenylalanine ammonia-lyase (PAL),whose increased activity leads to the accumulation of phenoliccompounds (e.g., chlorogenic acid, dicaffeoyl tartaric acid, andisochlorogenic acid) and tissue browning (Salveit, 2000). Inhi-bition of PAL synthesis appears to result from the redirection ofprotein synthesis away from wound-induced proteins to the syn-thesis of HSPs. The effect of heat shock (45◦C for 90 s followedby rapid cooling to 0◦C) either 4 h before wounding or 2 h af-ter wounding was so persistent that the fresh-cut lettuce did notshow any browning after 15 days in air at 5◦C (Salveit, 2000).However, it has also been shown that this treatment was not suc-cessful in tissues with constitutively or induced high levels ofphenolic compounds. The heat shock acts only on the synthesisof PAL and not on the activity of other enzymes involved intissue browning (Salveit, 2000).

DROUGHT STRESS AND DESICCATION TOLERANCE

Water deficit can be defined as any water content of a tissueor cell that is below the highest water content exhibited in themost hydrated state (Taiz and Zeiger, 2002). Lack of water hasseveral detrimental effects on plants, including modification ofthe cell wall crystallinity, clumping of microfibrils, denaturationof proteins, loss of cell turgor and membrane fluidity, and oxida-tive damage by reactive oxygen species (Aguilera et al., 2003;Prothon et al., 2003).

Strategies for Desiccation Tolerance

Some plant tissues can acquire desiccation tolerance, definedas the ability to function while dehydrated, or desiccation post-ponement, defined as the ability to maintain tissue hydration(Davies, 2004). Desiccation tolerance involves a co-ordinatedset of mechanisms that help certain tissues to survive dehydra-tion. These mechanisms include stomatal closure (Davies et al.,2002), osmotic adjustment, removal of reactive oxygen species,and the accumulation of late embryogenesis-abundant (LEA)proteins (Oliver et al., 2001).

Plants can continue to take up water only when their waterpotential is below that of the water source. Osmotic adjust-ment, in which cells accumulate osmotically active solutes (alsoknown as compatible solutes or osmolytes and including sugars,organic acids, glycine betaine, sorbitol, proline, amino acids,polyols, quaternary amines, and ions), is a process in which thewater potential of the tissue can be decreased without an accom-panying decrease in turgor (see Gomez et al., 2004 for definitionsof plant water relations). The change in tissue water potentialresults simply from changes in the osmotic potential (Fan et al.,1994; Zhang et al., 1999). In radish tubers the total concentrationof free sugars increases with soil water deficit (Herppich et al.,

2001a). During storage, carrots can increase their concentrationof glucose and fructose from their sucrose stores (Herppichet al., 2001b,c). These monosaccharides contribute twice asmuch to osmotic pressure per unit weight as disaccharides.

Cellular electron transport chains are impaired upon dehy-dration and may generate increasing amounts of reactive oxygenspecies (Hoekstra, 2002). Free radical attack on phospholipids,DNA and proteins is one of the molecular mechanisms ofdamage leading to death in desiccation-sensitive cells upondrying (Oliver et al., 2001). Protection against ROS is thoughtto play a role in desiccation tolerance. Therefore, free radicalscavenging systems are important components among themechanisms governing desiccation tolerance. Over-expressionof some enzymes, such as manganese superoxide dismutaseand glutathione S-transferase/glutathione peroxidase, has beenassociated with an enhanced tolerance to water deficit in trans-genic tobacco plants and cotton cells (Serrano and Montesinos,2003). Moreover, desiccation-tolerant organisms (seeds) canreduce and adapt their metabolic activities early during dryingto decrease the generation of ROS (Leprince et al., 1994).

Stress often induces the accumulation of proteins, as has beendescribed for AFPs in the case of low-temperature stress andHSPs in heat stress. In the case of drought stress, a large groupof genes code for hydrophilic LEA proteins, which are sus-pected to play a role in the acquisition of desiccation tolerance(Blackman et al., 1995). Although the function of LEA proteinsis not well-understood, they accumulate in vegetative tissuesduring episodes of drought. Their protective role may beassociated with their ability to retain water and to preventcrystallization of cellular proteins during desiccation (Serranoand Montesinos, 2003). Oliver et al. (2001), summarize thepossible protective roles of LEA proteins. At high hydrationlevels, LEA proteins might play a role in sequestering ions andpreventing of the damaging effects of free radical reactions.In the dried state, LEA proteins may act together with carbo-hydrates in the formation of a tight hydrogen-bound network,providing stability to macromolecular and cellular structuresin the cytoplasm. This network would inhibit the fusion ofcellular membranes, denaturation of cytoplasmic proteins, andthe detrimental effects of free radical reactions.

Drought typically leads to the accumulation of ABA. Numer-ous genes are induced by both drought and ABA accumulationduring the stress episode (Liu et al., 2005). Exogenous applica-tion of ABA has been shown to induce desiccation tolerance insomatic alfalfa embryos. Heat shock pretreatment, at 38◦C foras little as 10 min, induced a degree of desiccation tolerance inthe somatic embryos which was equivalent to ABA applicationand was therefore shown to be a viable alternative to exogenousABA treatment. The drying rate did not influence the survivalof the heat-stressed embryos (Senaratna et al., 1989).

Application to Food Dehydration

The quality of air-dehydrated plant products is often very low,with shrunken, shrivelled, darkened tissue, and poor rehydration

Page 11: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 759

ability (Nijhuis and Torringa, 1996). Over the years, techniquessuch as freeze-drying and vacuum drying have been developedin attempts to improve the characteristics of the dried material.However, much remains to be done if we are to attain high qualitycharacteristics of semi-prepared fruit and vegetables (Prothon,2002) regarding color, texture, and the appearance of freshnessof rehydrated products (Serrano and Montesinos, 2003). Pro-cesses should be optimized so as to prevent tissue damage. Thequality of the product will be associated with the preservationof the structure and the function of biological membranes andproteins during desiccation, storage, and rehydration (Serranoand Montesinos, 2003).

To the best of our knowledge, no application of the principlesof desiccation tolerance described above to food dehydration hasbeen reported. Few studies have pointed out that a better under-standing of the mechanisms by which desiccation-tolerant or-ganisms survive desiccation may lead to the development of newmethods of preserving foods and biological materials. Furtherresearch is therefore needed on the following topics:

• The use of glass-forming carbohydrates. Aguilera and Karel(1995) and Aguilera (2003) highlighted the importance ofsearching for carbohydrates, e.g. trehalose (which appearsto be the preferred sugar synthesized before dehydration ofyeasts, fungi and bacteria) or sucrose, raffinose, stachyose andverbascose (with an analogous role in seeds of higher plants)to preserve food materials as low-moisture glasses. Survivalunder desiccation has been suggested to be associated with vit-rification of the cytoplasm (Aguilera and Karel, 1995). In theglassy state, the molecular mobility and biochemical activityare restricted in the cytoplasm, and possibly in key organelles,but normal activities resume upon rehydration (Williams andLeopold, 1989).

• The application of stress pretreatment aimed at inducing cer-tain levels of desiccation tolerance (cross-tolerance). Heatstress has been suggested as an effective method of achiev-ing this aim (Senaratna et al., 1989; Tunnacliffe et al., 2001).The effect of cold stress could also be investigated. Plant tis-sue acclimated to cold implies protection of cell membranesagainst dehydration (in this case the intended protection isagainst freezing-induced dehydration) and an increase in thestrength of cell wall (which may help to prevent tissue collapse(Prothon et al., 2003)).

• The combination of the above, alone or together with dif-ferent processing technologies. The combination of osmoticand microwave dehydration or calcium pretreatment prior tomicrowave-assisted dehydration (Prothon et al., 2001; Ahrneet al., 2003) could be applied after stress pre-treatment or ap-plication of glass-forming carbohydrates.

• Genetic engineering it can be used to generate transgenicplants suitable for growth under drought conditions and des-tined for the production of dried foods (Aguilera et al., 2003;Serrano and Montesinos, 2003). The question here is whethertransgenic products will be accepted by consumers.

FUTURE PERSPECTIVES

The carbon and oxygen metabolism of plant cells is connectedto several processes of which we have limited understanding.These include ROS metabolism and signalling, cell survival,stress resistance, and redox homeostasis. Industrial practices in-volved, for example, in the production of minimally processedfruit and vegetables are likely to influence these metabolic pro-cesses and, therefore, research is needed to gain knowledge onnovel (i.e. not found in nature) tissue stress conditions duringprocessing operations in the food industry.

For example, packaging in a modified atmosphere may affectthe metabolism of the product, influencing storage and qualityproperties. Jacobsson (2004) demonstrated that different levelsof O2 and CO2 in the package affect the metabolism of broccoli,resulting in changes in the aroma, which, in many cases, werenot noticeable until after the broccoli was cooked. Plant stressresponses often involve changes in secondary metabolism. It cannot be excluded that factors affecting primary metabolism, suchas the exposure to different atmospheres inside the package, canaffect secondary metabolic pathways involved in the productionof aroma compounds.

Recent publications on novel processing techniques such asthe application of high hydrostatic pressure or pulsed electricfields (Dornenburg and Knorr, 1998; Ye et al., 2004) have sug-gested the possibility of using these techniques to stress the cellsand stimulate secondary metabolism and thus the biosynthesisof desirable health-promoting metabolites.

External application of substances used in the food indus-try to prevent enzymatic browning, such as citric acid and L-cysteine (Laurila et al., 1998), is another example of novelstress conditions occurring due to industrial practices. Cys-teine induced severe down-regulation of the cytochrome path-way followed by the induction of alternative oxidase (AOX)expression in tobacco cells (Vanlerberghe et al., 2002). In cellswith suppressed AOX expression, the application of cysteineeven induced programmed cell death. At neutral pH, citrate hasbeen shown to increase AOX expression in cell suspensions po-tentially increasing respiratory catabolism (Vanlerberghe andOrdog, 2002). However, the consequences of cell metabolismresulting from the application of cysteine and citrate are not well-understood. Citric acid application would cause acidic stress tothe cells by lowering the apoplastic pH below normal levels,and a decrease in pH has been shown to increase gene expres-sion of alternative respiratory pathways, including AOX (Esco-bar et al., 2006). According to Lambers et al. (1998) the tissuecopes with excess H+ uptake at low pH by increasing activeH+ pumping by plasma membrane ATPases, increasing the de-mand for respiratory energy. Therefore, changes in metabolicactivity due to the application of anti-browning substances inthe food industry must be understood at the gene expressionlevel with regard to the consequences on rates of oxygen con-sumption, browning inhibition, sugar metabolism, and cell wallchanges during wound-induced reactions in fresh-cut fruit andvegetables.

Page 12: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

760 F. G. GALINDO ET AL.

Investigations of the genetic control of metabolism duringindustrial processing of fresh fruit and vegetables, through tech-niques such as transcriptomics and metabolic profiling, will pro-vide knowledge on the consequences of industrial practices es-sential for quality assurance and optimization.

REFERENCES

Aguilera, J. M. and Ballivian, A. (1987). A kinetic interpretation of texturalchanges in black beans during prolonged storage. Journal of Food Science,52:691–695.

Aguilera, J. M. and Karel, M. (1995). Preservation of biological materials underdesiccation. Critical Reviews in Food Science and Nutrition, 37:287–309.

Aguilera, J. M. (2003). Drying and dried products under the microscope. FoodScience and Technology International, 9:137–143.

Aguilera, J. M., Chiralt, A., and Fito, P. (2003). Food dehydration and productstructure. Trends in Food Science and Technology, 14:432–437.

Ahn, Y. J., Claussen, K., and Zimmerman, L. (2004). Genotypic differences inthe heat-shock response and thermotolerance in four potato cultivars. PlantScience, 166:901–911.

Ahrne, L., Prothon, F., and Funebo, T. (2003). Comparison of drying kineticsand texture effects of two calcium pre-treatments before microwave assisteddehydration of apple and potato. International Journal of Food Science andTechnology, 38:411–420.

Ahvenainen, R. (1996). New approaches in improving the shelf life of minimallyprocessed fruits and vegetables. Trends in Food Science and Technology,7:179–186.

Alamillo, J., Almoguera, C., Bartles, D., and Jordano, J. (1995). Constitutiveexpression of small heat shock proteins in vegetative tissues of the resurrectionplant Craterostigma plantagineum. Plant Molecular Biology, 29:1093–1099.

Anthon, G. E. and Barrett, D. M. (2006). Characterization of the temperatureactivation of pectin methylesterase in green beans and tomatoes. Journal ofthe Agricultural and Food Chemistry, 54:204–211.

Aroca, R., Irigoyen, J. J. and Sanchez-Dıaz, M. (2003). Drought enhances maizechilling tolerance.II. Photosynthetic traits and protective mechanisms againstoxidative stress. Physiologia Plantarum, 117:540–549.

Atkin, O. K. and Tjoelker, M. G. (2003). Thermal acclimation and the dynamicresponse of plant respiration to temperature. Trends in Plant Science, 8:343–351.

Banzet, N., Richaud, C., Deveaux, Y., Kazmaier, M., Gagnon, J., andTriantaphylides, C. (1998). Accumulation of small heat shock proteins, in-cluding mitochondrial HSP22, induced by oxidative stress and adaptive re-sponse in tomato cells. Tha Plant Journal, 13:519–527.

Barry-Ryan, C and O’Beirne, D. (1997). Unit operations in processing ready-to-use vegetable products. Report September 1997, Unit Operations in Pro-cessing, University of Linmerk-Ireland.

Barry-Ryan, C. and O’Beirne, D. (1998). Quality and shelf-life of fresh cutcarrot slices as affected by slicing method. Journal of Food Science, 63:1–6.

Barry-Ryan, C. and O’Beirne, D. (2000). Effects of peeling methods on thequality of ready-to-use carrot slices. International Journal of Food Scienceand Technology, 35:243–254.

Bartolome, L. G. and Hoff, J. E. (1972). Firming of potatoes: biochemical effectsof peheating. Journal of the Agricultural and Food Chemistry, 20:266–270.

Ben-Yehoshua, S. (2003). Effects of postharvest heat and UV applications ondecay, chilling injury and resistance agains pathogenes of citrus and otherfruits and vegetables. Acta Horticulturae, 599:159–173.

Bernards, M. A., Fleming, W. D., Llewellyn, D. B., Priefer, R., Yang, X.,Sabatino, A. and Plourde, G.L. (1999). Biochemical characterization ofthe suberization-associated anionic peroxidase of potato. Plant Physiology,121:135–145.

Biddington, N. L. and Dearman, A. S. (1985). The effect of mechanically inducedstress on the growth of cauliflower, lettuce and celery seedlings. Annals ofBotany, 55:109–119.

Blackman, S. A., Obendorf, R. L., and Leopold, A. C. (1995). Desiccation tol-erance in developing soybeans seeds: The role of stress proteins. PhysiologiaPlantarum, 93:630–638.

Blenkinsop, R. W., Yada, R. Y., and Marangoni, A. G. (2004). Metabolic controlof low-temperature sweetening in potato tubers during postharvest storage.Horticultural Reviews, 30:317–354.

Bolwell, G. P., Butt, V. S., Davies, D. R., and Zimmerlin, A. (1995). The originof the oxidative burst in plants. Free Radical Research, 6: 517–532.

Boyer, J. S. (1982). Plant productivity and environment. Science, 218:443–448Bowen, J., Lay-Yee, M., Plummer, K., and Ferguson, I. (2002). The heat shock

response is involved in thermotolerance in suspension-cultured apple fruitcells. Journal of Plant Physiology, 159:599–606.

Bradley, D. J., Kjelbom, P., and Lamb, C.J. (1992). Elicitor-and wound-inducedoxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapiddefense response. Cell, 70:21–30.

Breton, G., Danyluk, J., Ouellet, F., and Sarhan, F. (2000). Biotechnologicalapplications of plant freezing associated proteins. Biotechnology Annual Re-view, 6:59–101.

Brierley, E. R., Bonner, P. L. R., and Cobb, A. H. (1996). Factors influencingthe free amino acid content of potato (Solanum tuberosum L.) tubers duringprolonged storage. Journal of the Science of Food and Agriculture, 70:515–525.

Brodl, M. R. and Ho, T. D. (1992). Heat shock in mechanically wounded carrotroot disks causes destabilization of stable secretory protein mRNA and disso-ciation of endoplasmic reticulum lamellae. Physiologia Plantarum, 86:253–262.

Chang, Y. and Reed, B. M. (2000). Extended alternating-temperature cold ac-climation and culture duration improve pear shoot cryopreservation. Cryobi-ology, 40:311–322.

Charron, C. S. and Cantliffe, D. J. (1995). Volatile emissions from plants. Hor-ticultural Reviews, 17:43–71.

Chuda, Y., Ono, H., Yada, H., Ohara-takada, A., Matsuura-Endo, C., and Mori,M. (2003). Effects of physiological changes in potato tubers (Solanum tubero-sum L.) after low temperature storage on the level of acrylamide formed inpotato chips. Bioscience, Biotechnology, and Biochemistry, 67:1188–1190.

Chun, J. U., Yu, X. M., and Griffith, M. (1998). Genetic studies of antifreeze pro-teins and their correlation with winter survival in wheat. Euphytica, 102:219–226.

Clarkson, G. J. J., O’Byrne, E. E., Rothwell, S. D., and Taylor, G. (2003).Identifying traits to improve postharvest processability in baby leaf salad.Postharvest Biology and Technology, 30:287–298.

Cooper, P. and Ho, T. D. 1983. Heat-shock proteins in maize. Plant Physiology,71:215–222.

Danyluk, J., Perron, A., Hounde, M., Limin, A., Fowler, B., Benhamou, N., andSarhan, F. (1998). Accumulation of an acidic dehydrin in the vicinity of theplasma membrane during cold acclimation of wheat. Plant Cell, 10:623–638.

Davies, M. (2004). Functional genomics of drought stress responses in plants:A review. Physiology and Molecular Biology of Plants, 10:29–36.

Davies, W. J., Wilkinson, S., and Loveys, B. (2002). Stomatal control by chem-ical signaling and the exploitation of this mechanism to increase water-useefficiency in agriculture. New Phytologist, 153:449–460.

De Belie, N., Herppich, W., and De Baerdemaeker, J. (2000). Turgor changesin red cabbage during mild heat treatment. Journal of Plant Physiology,157:263–272.

De Rocher, A. E., Helm, K. W., Lauzon, L. M., and Vierling, E. (1991). Expres-sion of a conserved family of cytoplasmic low molecular weight heat-shockproteins during heat stress and recovery. Plant Physiology, 96:1038–1047.

Deiting, U., Zrenner, R., and Stitt, M. (1998). Similar temperature requirementfor sugar accumulation and for the induction of new forms of sucrose phos-phate synthase and amylase in cold-stored potato tubers. Plant Cell Environ-ment, 21:127–138.

Dornenburg, H. and Knorr, D. (1998). Monitoring the impact of high-pressureprocessing on the biosynthesis of plant metabolites using plant cell cultures.Trends in Food Science and Technology, 9: 355–361.

Duman, J. G. and Olsen, T. M. (1993). Thermal hysteresis protein-activity inbacteria, fungi and phylogenetically diverse plants. Cryobiology, 30:322–328.

Page 13: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 761

Escobar, M. A., Geisler, D. A., and Rasmusson, A. G. (2006). Reorganizationof the alternative pathways of the Arabidopsis respiratory chain by nitrogensupply: opposing effects of ammonium and nitrate. Plant Journal, 45:775–788.

Espen, L., Morgutti, S., Abruzzese, A., Negrini, N., Rivetta, A., Quattrini, M.M., Cocucci, M., and Cocucci, S. M. (1999). Changes in the potato (Solanumtuberosum L.) tuber at the onset of dormancy and during storage at 23◦C and3◦C. I. Biochemical and physiological parameters. Potato Research, 42:189–201.

Fallik, E., Grinberg, S., Alkalai, S., Yekutieli, O., Wiseblum, A., Regev, R.,Beres, H., and Bar-Lev, E. (1999). A unique rapid hot water treatment toimprove storage quality of sweet pepper. Postharvest Biology and Technology,15:25–32.

Fan, S., Blake, J., and Blumwald, E. (1994). The relative contribution of elasticand osmotic adjustments to turgor maintenance of woody species. PhysiologiaPlantarum, 90:408–413.

Faure-Mlynski, M., Aharoni, N., Mayak, S., and Lers, A. (2004). Mode of actionof heat treatment applied to sweet Basil (Ocimum basilicum) for reduction ofchilling injury. Acta Horticulturae, in press.

Feeney, R. E. and Yeh, Y. (1993). Antifreeze proteins: properties, mechanismsof action and possible applications. Food Technology, 1:82–88.

Fletcher, G., Goddard, S. V., and Wu, Y. (1999). Antifreeze proteins and theirgenes: from basic research to business opportunity. Chemtech, 6:17–28.

Friedman, M. (1997). Chemistry, biochemistry, and dietary role of potatopolyphenols. A review. Journal of Agricultural and Food Chemistry, 45:1523–1540.

Fu, P., Wilen, R. W., Wu, G. H., Robertson, A. J., and Gusta, l. V. (2000).Dehydrin gene expression and leaf water potential differs between spring andwinter cereals during cold acclimation. Journal of Plant Physiology, 156:394–400.

Gaspar, T., Franck, T., Bisbis, B., Kevers, C., Jouve, L., Hausman, J. F., andDommes, J. (2002). Concepts in plant stress physiology: Application to planttissue cultures. Plant Growth Regulation, 37:263–285.

George, M. F. and Burke, M. J. (1977). Cold-hardiness and deep supercoolingin xylem of shagbark hickory. Plant Physiology, 27:507–528.

George, M. F., Beckwar, M. R., and Burke, M. J. (1982). Freezing avoidanceby deep undercooling of tissue water in winter-hardy plants. Cryobiology,19:628–638.

Gomez, F. (2004). Physiological and Biochemical Aspects of Vegetable process-ing. A Case Study on Carrots. Ph.D. Thesis. Lund University, Food Engineer-ing Dept. Sweden.

Gomez, F. and Sjoholm, I. (2004). Applying biochemical and physiologicalprinciples in the industrial freezing of vegetables: a case study on carrots.Trends in Food Science and Technology, 15:39–43.

Gomez, F., Herppich, W., Gekas, V., and Sjoholm, I. (2004). Factors affectingquality and postharvest properties of vegetables: Integration of water relationsand metabolism. Critical Reviews in Food Science and Nutrition, 44:139–154.

Gonzalez-Martınez, G. (2003). Heat induced cell membrane injury of vegetabletissues - an applied study on potatoes. Ph.D. Thesis, Food Engineering De-partment, Lund University, Sweden.

Graham, D. and Patterson, B. D. (1982). Responses of plants to low, nonfreezingtemperatures: Proteins, metabolism, and acclimation. Annual Reviews in PlantPhysiology, 33:347–372.

Griffith, M., Ala, P., Yang, D. S. C., Hon, WC, and Moffatt. B. A. (1992).Antifreeze protein produced endogenously in winter rye leaves. Plant Physi-ology, 100:593–596.

Griffith, M. and Antikainen, M. (1996). Extracellular ice formation in freezing-tolerant plants. In: Advances in Low-Temperature Biology. pp. 107–139. Vol.3. JAI Press Inc.

Griffith, M. and Ewart, K. V. (1995). Antifreeze proteins and their potential usein frozen foods. Biotechnology Advances, 13:375–402.

Hansen, L. D., Afzal, M., Breidenbach, R. W., and Criddle, R. S. (1994). High-and low-temperature limits to growth of tomato cells. Planta, 195:1–9.

Hart, P. C. M., Pallett, K. E., and Cobb, H. (1986). Metabolic changes in PentlandDell tubers during storage at 5◦C and 10◦C. Aspects of Applied Biology,13:457–465.

Herppich, W. B., Mempel, H., and Geyer, M. (1999). Effects of postharvestmechanical and climatic stress on carrot tissue water relations. PostharvestBiology and Technology, 16:43–49.

Herppich, W. B., Linke, M., Landahl, S., and Gzik, A. (2001a). Pre-harvest andpostharvest responses of radish to reduced water supply during growth. In:Proceedings of the fourth International Conference on Postharvest Science,Jerusalem, Israel. Acta Horticulturae, 553: 89–90.

Herppich, W. B., Mempel, H., and Geyer, M. (2001b). Osmotic and elasticadjustment, and product quality in cold-stored carrots roots (Daucus carotaL.). Gartenbauwissenschaft, 66:20–26.

Herppich W. B., Mempel, H., and Geyer, M. (2001c). Drought- and lowtemperature-acclimation in carrot (Daucus carota L.) roots. Journal of Ap-plied Botany, 75:138–143.

Hoekstra, F. A. (2002). Role of respiration in desiccation tolerance.www.plantphys.net Essay 11.5.

Hoffmann, T. and Wormanns, G. (2002). Determination of material charac-teristics of potatoes regarding processing and consumption—impact stressand tendency to develop black spots. In Proceedings of the 6th internationalsymposium on friut, nut, and vegetable production engineering. Potsdam,Germany. pp. 397–401.

Hoisydai, S. and Harrington, H. M. (1989). Characterization of the heat-shockresponse in cultured sugarcane cells. Plant Physiology, 90:1156–1162.

Houde, M., Daniel, C., Lachapelle, M., Allard, F., Laliberte, F., and Sarhan, F.(1995). Immunolocalisation of freezing-tolerance associated proteins in thecytoplasm and nucleous of wheat crown tissues. Plant Journal, 8:583–593

Hsieh, M., Chen, J., Jinn, T., Chen, Y., and Lin, C. (1992). A class of soybeanlow molecular weight heat-shock proteins. Plant Physiology, 99:1279–1284.

Jacobsson, A. (2004). Quality aspects of modified atmosphere packed broccoli.Ph.D. Thesis. Lund University, Food Engineering Dept. Sweden.

Jaitrong, S., Rattanapanone, N., Boonyakiat, D., and Baldwin, E. (2004). Acomparison of anatomical changes between normal and chilling-injured Lo-gan fruit pericarp. Acta Horticulturae, in press.

Johnson, S. M., Doherty, S. J., and Croy, R. R. D. (2003). Biphasic superox-ide generation in potato tubers. A self-amplifying response to stress. PlantPhysiology, 131:1440–1449.

Joyce, S. M., Cassells, A. C., and Jain, S. M. (2003). Stress and aberrant phe-notypes in in vivo culture. Plant, Cell and Organ Culture , 74:103–121.

Kaack, K., Larsen, E., and Thybo, A. K. (2002a). The influence of mechanicalimpact and storage conditions on subsurface hardening in pre-peeled potatoes(Solanum tuberosum L.). Potato Research, 45: 1–8.

Kaack, K., Kaaber, L., Larsen, E., and Thybo, A. K. (2002b). Microstructural andchemical investigation of subsurface hardened potatoes (Solanum tuberosumL.). Potato Research, 45:9–15.

Kluge, M., Kliemchen, A., and Galla, H. J. (1991). Temperature effects onCrassulacean acid metabolism: EPR spectroscopic studies on the thermotropicphase behaviour of the tonoplast membranes of Kalanchoe diagremontiana.Botanica Acta, 104:355–360.

Knight, C. A. and Duman, J. G. (1986). Inhibition of recrystallization of ice byinsect thermal hysteresis proteins: a possible cryoprotective role. Cryobiology,23:256–262.

Lafuente, M. T., Belver, A., Guye, M. G., and Saltveit, M. E. (1991). Effect oftemperature conditioning on chilling injury of cucumber cotyledons. PlantPhysiology, 95:443-449.

Lambers, H., Chapin III, F. S. and Pons, T. L. (1998). Plant Physiological Ecol-ogy. New York, Springer.

Laties, G. G. (1978). The development and control of respiratory pathways inslices of plant storage organs. In Biochemistry of Wounded Plant Tissues. pp.421–466. Kahl, G. Ed. de Gruyter, New York.

Laurila, E., Kervinen, R., and Ahvenainen, R. (1998). The inhibition of enzy-matic browning in minimally processed vegetables and fruits. PostharvestNews and Information, 9:53–66.

Lee, C. Y., Bourne, M. C. and Van Buren, J. P. (1979). Effect of blanchingtreatments on the firmness of carrots. Journal of Food Science, 44:615–616.

Leprince, O., Atherton, N. M., Deltour, R., and Hendry, G. A. F. (1994). Theinvolvement of respiration in free radical processes during loss of desiccationtolerance in germinating Zea mays L. Plant Physiology, 104:1333–1339.

Page 14: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

762 F. G. GALINDO ET AL.

Liu, F., Jensen, C. R., and Andersen, M. N. (2005). A review of drought adapta-tion in crop plants: changes in vegetative and reproductive physiology inducedby ABA-based chemical signals. Australian Journal of Agricultural Research, 56:1245–1252.

Loaiza-Velarde, J. G., Tomas-Barbera, F. A., and Saltveit, M. E. (1997). Ef-fect of intensity and duration of heat shock treatments on wound-inducedphenolic metabolism in iceberg lettuce. Journal of the American Society ofHorticultural Science, 122:873–877.

Lopez-Galvez, G., Salveit, M., and Cantwell, M. (1996). Wound-induced pheny-lalanine ammonia lyase activity: factors affecting its induction and correlationwith the quality of minimally processed lettuces. Postharvest Biology andTechnology, 9:223–233.

Lulai, E. C. and Corsini, D. L. (1998). Differential deposition of suberin phenolicand aliphatic domains and their roles in resistance to infection during potatotuber (Solanum tuberosum L.) wound-healing. Physiological and MolecularPlant Pathology, 53:209–222.

Lurie, S. (1998). Postharvest heat treatments of horticultural crops. HorticulturalReviews, 22:91–121.

Malik, M. K., Slovin, J. P., Hwang, C. H., and Zimmerman, J. L. (1999). Modifiedexpression of a carrot small heat shock protein gene, Hsp 17.7, results inincreases or decreased thermotolerance. The Plant Journal, 20:89–99.

Marangoni, A. G., Butuner, Z., Smith, J. L., and Stanley, D. W. (1990). Physicaland biochemical changes in the microsomal membranes of tomato fruit as-sociated with acclimation to chilling. Journal of Plant Physiology, 135:653–661.

Martin-Cabrejas, M. A. and Esteban, R. M. (1995). Hard-to-cook phenomenonin beans: changes in antinutrient factors and nitrogenous compounds duringstorage. Journal of the Science of Food and Agriculture, 69: 429–435.

Mempel, H. and Geyer, M. (1999). Influence of mechanical stresses on therespiration activity of carrots. Gartenbauwissenschaft, 64:118–125.

Miller, A. R. and Kelley, T. J. (1989). Mechanical stress stimulates peroxidaseactivity in cucumber fruit. HortScience, 24:650–652.

Miroshnichenko, S., Tripp, J., Nieden, U. Z., Neumann, D., Conrad, U., andManteuffel, R. (2005). Immunomodulation of function of small heat shockproteins prevents their assembly into heat stress granules and results in celldeath at sublethal temperatures. The Plant Journal 41:269–281.

Nijhuis, H. H. and Torringa, E. (1996). Research needs and opportunities in thedry conservation of fruits and vegetables. Drying Technology 14:1429–1457.

Oliver, A. E., Leprince, O., Wolkers, W. F., Hincha, D. K., Heyer, A. G., andCrowe, J. H. (2001). Non-disaccharide-based mechanisms of protection dur-ing drying. Cryobiology, 43:151–167.

Palta, J. P. (1990). Stress interactions at the cellular and membrane levels.HortScience, 25:1377–1381.

Palta, J. P., Whitaker, B. D., and Weiss, L. S. (1993). Plasma membrane lipidsassociated with genetic variability in freezing tolerance and cold acclimationof Solanum species. Plant Physiology, 103:793–803.

Parkin, K. L., Marangoni, A., Jackman, R. L., Yada, R. Y. and Stanley, D. W.(1989). Chilling injury, a review of possible mechanisms. Journal of FoodBiochemistry, 13:127–153.

Pearce, R. S. (2001). Plant freezing and damage. Annals of Botany, 87:417–424.Pena-Cortes, H. and Willmitzer, L. (1995). The role of hormones in gene acti-

vation in response to wounding. In: Plant Hormones. pp. 395–414. Davies,P.J., Ed., Kluwer Academic Press.

Pilnik, W. and Voragen, A. G. J. (1991). The significance of endogenous andexogenous pectic enzymes in fruit and vegetable processing. In: Food Enzy-mology. p. 303. Fox, P.E., Ed., Elsevier, London.

Potato Marketing Board. (1994). Facsheet 1. Potato Marketing Board, Cowley,UK.

Prasad, T. K. (1996). Mechanisms of chilling-induced oxidative stress injuryand tolerance in developing maize seedlings: changes in antioxidant system,oxidation of proteins and lipids, and protease activities. The Plant Journal,10:1017–1026.

Prothon, F, Ahrne, L., Funebo, F., Kidman, S, Langton, M., and Sjoholm,I. (2001). Effects of combined osmotic and microwave dehydration of ap-ple on texture, microstructure and rehydration characteristics. Lebensmittel-Wissenshaft und Technologi, 34:95–101.

Prothon, F. (2002). Combined dehydration methods. From fresh fruit to high-quality ingredients. Ph.D. Thesis. Lund University, Food Engineering Dept.Sweden.

Prothon, F., Ahrne, L., and Sjoholm, I. (2003). Mechanisms and prevention ofplant tissue collapse during dehydration. Critical Reviews in Food Scienceand Nutrition, 43:447–479.

Purvis, A. and Shewfelt, R. L. (1993). Does the alternative pathway amelioratechilling injury in sensitive plant tissue?. Physiologia Plantarum, 88:712–718.

Pontinen, V. and Voipio, I. (1992). Different methods of mechanical stress incontrolling the growth of lettuce and cauliflower seedlings. Acta AgricolaScandinavica, 42:246–250.

Ramakrishna. W., Deng, Z., Ding, C. K., Handa, A. K., and Ozminkowski,R. H. (2003). A novel small heat shock protein gene, vis1, contributes topectin depolymerization and juice viscosity in tomato fruit. Plant Physiology,131:725–735.

Razem, F. and Bernards. M. A. (2002). Hydrogen peroxide is required forploy(phenolic) domain formation during wound-induced suberization. Jour-nal of Agricultural and Food Chemistry, 50:1009–1015.

Razem, F. and Bernards. M. A. (2003). Reactive oxygen species productionin association with suberization: evidence for a NADPH-dependent oxidase.Journal of Experimental Botany, 54:935–941.

Reyes-Moreno, C. and Paredes-Lopez, O. (1993). Hard-to-cook phenomenon incommon beans—A review. Critical Reviews in Food Science and Nutrition,33:227–286.

Roe, M. A., Faulks, R. M., and Belsten, J. L. 1990. Role of reducing sugarsand amino acids in fry colour of chips from potatoes grown under differentnitrogen regimes. Journal of the Science of Food and Agriculture, 52:207–214.

Rosen, J. and Hellenas, K. E. (2002). Analysis of acrylamide in cooked foodsby liquid chromatography tandem mass spectrometry. Analyst, 127:880–882.

Rutherford, P. P. (1981). Some biochemical changes in vegetables during storage.Annals of Applied Biology, 98:538–541.

Sabehat, A., Weiss, D., and Lurie, S. (1996). The correlation between heat-shockprotein accumulation and persistence and chilling tolerance in tomato fruit.Plant Physiology, 110:531–537.

Saltveit, M.E. (2000). Wound induced changes in phenolic metabolism and tissuebrowning are altered by heat shock. Postharvest Biology and Technology,21:61–69.

Satoh, S., Sturm, A., Fujii, T., and Crispeels, M. J. (1992). cDNA cloning of anextracellular dermal glycoprotein of carrot and its expression in response towounding. Planta, 188:432–438

Seljasen, R., Bengtsson, G. B., Hoftun, H., and Vogt, G. (2001). Sensory andchemical changes in five varieties of carrot (Daucus carota L) in response tomechanical stress at harvest and post-harvest. Journal of the Science of Foodand Agriculture, 81:436–447.

Senaratna, T., McKersie, B. D. and Bowley, S. R. (1989). Desiccation tol-erance of alfalfa (Medicago sativa L.) somatic embryos. Influence of ab-scisic acid, stress pretreatments and drying rates. Plant Science, 65:253–259.

Serrano, R. and Montesinos, C. (2003). Molecular bases of desiccation tolerancein plant cells and potential applications in food dehydration. Food Science andTechnology International, 9:157–161.

Shattuck, V. I., Kakuda, Y., and Yada, R. (1989). Sweetening of parsnip rootsduring short-term cold storage. Canadian Institute of Food Science and Tech-nology Journal, 22:378–382.

Showalter, A. M. and Varner, J. E. (1987). Molecular details of plant cell wallhydroxyproline-rich glycoprotein expression during wounding and infection.In: Molecular Strategies for Crop Protection. pp. 375–392. Arntzen, C. J. andRyan, C., Eds., Alan R Liss, New York.

Smallwood, M., Worrall, D., Byas, L., Elias, L., Ashford, D., Doucet, Ch. J.,Holt, Ch., Telford, L., Lillford, P., and Bowles, D. J. (1999). Isolation andcharacterization of a novel antifreeze protein from carrot (Daucus carota).Biochemical Journal, 340:385–391.

Smallwood, M. and Bowles, D. J. (2002). Plants in a cold climate. PhilosophicalTransactions of the Royal Society of London. Series B: Biological Sciences,357:831–847.

Page 15: 2007 plant stress physiology- opportunities and challenges for the food industry

Dow

nloa

ded

By:

[Cho

nnam

Nat

iona

l Uni

vers

ity] A

t: 02

:36

7 A

pril

2008

PLANT STRESS PHYSIOLOGY 763

Stanley, D. W. (1991). Biological membrane deterioration and associated qualitylosses in food tissues. Critical Reviews in Food Science and Nutrition, 30:487–553.

Steponkus, P. L. (1984). Role of the plasma membrane in freezing injury andcold acclimation. Annual Review of Plant Physiology and Plant MolecularBiology, 35:543–584

Stolle-Smits, T., Beekhuizen, J. G., Recourt, K., Voragen, A. G. J., and VanDijk, C. (2000). Preheating effects on the textural strength of canned greenbeans. 1. Cell wall chemistry. Journal of the Agricultural and Food Chemistry48:5269–5277.

Surjadinata, B. B. and Cisneros-Zevallos, L. (2003). Modelling wound-inducedrespiration of fresh-cut carrots (Daucus carota L.). Journal of Food Science,68:2735–2740.

Taiz, L. and Zeiger, E. (2002). Plant Physiology. 3rd edition. Sinauer AssociatesInc. Sunderland.

Tareke, E., Rydberg, P., Karlsson, P., Eriksson, S., and Tornqvist, M. (2002).Analysis of acrylamide, a carcinogen formed in heated foodstuffs. Journal ofAgricultural and Food Chemistry, 50:4998–5006.

Thomashow, M. F. (1999). Plant Cold Acclimation: freezing tolerance genesand regulatory mechanisms. Annual Reviews in Plant Physiology and PlantMolecular Biology, 50:571–599.

Tronsmo, A. M. (1986). Host water potentials may restrict development of snowmold fungi in low temperature hardened grasses. Physiologia Plantarum,68:175–179.

Tunnacliffe, A., Garcıa, A., and Manzanero, M. (2001). Anhydrobiotic engineer-ing of bacterial and mammalian cells: Is intracellular trehalose sufficient?.Cryobiology, 43:124–132.

Ukaji, N., Kuwabara, C., Takezawa, D., Arakawa, K., and Fujikawa, S. (2001).Cold acclimation-induced WAP27 localized in endoplasmic reticulum in cor-tical parenchyma cells of mulberry tree was homologous to group 3 late-embryogenesis abundant proteins. Plant Physiology, 126:1588–1597.

Urrutia, M. E., Duman, J. G., and Knight, C. A. (1992). Plant thermal hysteresisproteins. Biochimica et Biophysica Acta, 1121:199–206.

Vandenbussche, B., Leuridan, S., Verdoodt, V., Gysemberg, M., and De Proft,M. (1999). Changes in sugar content and fatty acid composition of in vitrosugar beet shoots after cold acclimation: influence on survival after cryop-reservation. Plant Grow Regulation, 28:157–163.

Vanlerberghe, G. C., Robson, C. A., and Yip, J. Y. H. (2002). Induction ofmitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. PlantPhysiology, 129:1829–1842.

Vanlerberghe, G. C., and Ordog, S. H. (2002). Alternative oxydase: integratingcarbon metabolism and electron transport in plant respiration. In: Advances

in Photosynthesis and Respiration: Photosynthetic Nitrogen Assimilation andAssociated Carbon Metabolism. Foyer, C. H. Noctor G. (Eds). Kluwer Aca-demic Publishers, The Netherlands.

Veselov, A. P., Kurganova, L. N., Likhacheva, A. V. and Sushkova, U. A. (2002).Possible regulatory effect of lipid peroxidation on the H+-ATPase activity ofthe plasmalemma under stress conditions. Russian Journal of Plant Physiol-ogy, 49:344–348.

Vierling, E. (1991). The role of heat-shock proteins in plants. Annual Review inPlant Physiology and Plant Molecular Biology, 42:579–620.

Viswanathan, C. and Khanna-Chopra, R. (1996). Heat shock proteins—role inthermotolerance of crop plants. Current Science, 71:275–284.

Wadso, L, Gomez, F., Sjoholm, I., and Rocculi, P. (2004). Effect of tissue wound-ing on the results from calorimetric measurements of vegetable respiration.Thermochimica Acta, 422:89–93

Wang, C. Y., Bowen, J. H., Weir, I. E., Allan, A. C., and Ferguson, I. B.(2001). Heat-induced protection against death of suspension-cultured applefruit cells exposed to low temperature. Plant, Cell and Environment, 24:1199–1207.

Wehmeyer, N. and Vierling, E. (2000). The expression of small heat shockproteins in seeds responds to discrete developmental signals and suggests ageneral protective role in desiccation tolerance. Plant Physiology, 122:1099–1108.

Williams, R. J. and Leopold, A. C. (1989). The glassy state in corn embryos.Plant Physiology, 89:977–981.

Wismer, W. V., Marangoni, A. G., and Yada. R. Y. (1995). Low-temperaturesweetening in roots and tubers. Horticultural Reviews, 17:203–231.

Worrall, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Lillford,P., Telford, J, Holt, C., and Bowles, D. (1998). A carrot leucine-rich-repeatprotein that inhibits ice recrystallization. Science, 282:115–117.

Wurr, D. C. E., Fellows, J. R., and Hadley, P. (1986). The influence of sup-plementary lighting and mechanically-induced stress during plant raising, ontransplant and maturity characteristics of crisp lettuce. Journal of Horticul-tural Science, 61:325–330.

Ye, H., Huang, L. L., Chen, S. D., and Zhong, J. J. (2004). Pulsed electricfields stimulates plant secondary metabolism in suspension cultures of Taxuschinensis. Biotechnology and Bioengineering, 88:788–795.

Zhang, J., Nguyen, H. T., and Blum, A. (1999). Genetic analysis of osmoticadjustment in crop plants. Journal of Experimental Botany, 50:291–302.

Zykova, V. V., Grabelnykh, O. I., Tourchaninova, V. V., Antipina, A. I.,Koroleva, N. A., Kolesnichenko, A. V., Pobezhimova, T. P., Konstantinov,Y. M. and Voinikov, V. K. (2002). The effect of CSP310 on lipid peroxida-tion and respiratory activity in winter wheat mitochondria. Russian Journalof Plant Physiology, 49:628–634.