Improving Crop Resistance to Abiotic Stress (TUTEJA:PLANT STRESS OMICS O-BK) || Potato: Improving Crop Productivity and Abiotic Stress Tolerance

44Potato: Improving Crop Productivity and Abiotic Stress ToleranceGefu Wang-Pruski and Andrew Schofield

Potato is a prestige food crop that billions of people in the world depend on as anenergy source. Its widespread cultivation and adaptation have rendered it attractivefor humans of all cultures and geographic locations. However, its effective produc-tion is challenged by many unfavorable environmental conditions, such as drought,heat, cold, and salinity. Recent tools developed in genomic research have advancedour understanding of the potato crop in its ability to manage these stresses. Thischapter provides the latest information on our understanding of stress tolerancemechanisms inpotatoes based on functional genomics, transcriptomics, proteomics,and metabolomics studies. We also recommend many choices of functional genesthat can be used for improving stress tolerance in potatoes.Wewould like to point outthat due to lack of the completion of the potato genome sequence, many researchprojects are not able to providemore advanced systems biology data in comparison tothat available for many other agricultural species.

44.1Introduction

The potato crop (Solanum tuberosum L.) is ranked as the fourth food crop in the worldafter rice,wheat, andmaize (FAOSTAT). Its production in 2009 reached 329.6millionton with China as the top producer with 69 million ton, followed by India with 34million ton. A detailed, country-wise information on potato production, utilization,and trade can be found in the annually updated databases of theUnitedNations Foodand Agriculture Organization (FAO). The potato is a starchy, tuberous crop from theSolanaceae family known as the nightshades. It originated in the region of the Andesand was introduced to the rest of the world four centuries ago. Today, potatoes havebecome an integral part of much of the world cuisine due to their rich content ofcarbohydrates, proteins, vitamin C, iron, and fiber.

Potatoes are grown in about 100 countries, occupying every continent of the world.In some parts of the world, true botanical seeds are used to produce the crop,although most of the North American and European production systems rely ontuber seeds because of their genetic uniformity for traits such as size, color, texture,

Improving Crop Resistance to Abiotic Stress, First Edition.Edited by Narendra Tuteja, Sarvajeet Singh Gill, Antonio F. Tiburcio, and Renu Tuteja� 2012 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2012 by Wiley-VCH Verlag GmbH & Co. KGaA.

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and biochemical contents. Potatoes are used as fresh, processed, and value-addedfood products, as well as a source of industrial starch. The variety requirementsdepend on needs, including tuber shape and size, sugar content, frying color,nutritional value, storability, and disease resistance. The issues facing the industryare high acrylamide content in processed products, obesity related to consumption,and sustainable production systems for disease and pest control.

Nitrogen source is essential for tuber production. Nitrogen available to plants inthe soil and nitrogen loss in the system determine how much nitrogen is actuallyused by the plants. Because excesswater can lead to nutrient leaching, water becomesa key factor in determining how nitrogen can be taken up by plants. Estimation ofirrigation needs have been established in many countries based on the variety andclimate conditions. As precision farming for crop management increased in pop-ularity, effective nitrogen and water applications may be found in potato productionsystems around the world. Nevertheless, severe weather conditions and climatechange will continue to challenge the potato production systems in different parts ofthe world. Therefore, generation of new cultivars adapted to different stress condi-tions will become essential for potato production in the coming years.

44.2Potato Genomic Resources

Besides the cultivated potato (S. tuberosum ssp. tuberosum), other crops such astomato, pepper, eggplant, and tobacco are also keymembers of the Solanaceae family.Their genetic information is important for understanding the genome of potatoes.For instance, tomato (S. lycopersium) has a similar genome size to potato and is seen asa genetic and genomic model for the Solanaceae family. Cultivated potato behaves asan autotetraploid and has 2n¼ 4x¼ 48 chromosomes. It is generally understood thatpotato has a genome size of 850–1000Mb, which is very similar to that of tomato.However, a large number of wild and hybrid diploid selections are being used forgenetic mapping-related studies due to their reduced complexity of genome recom-bination. Nevertheless, the lack of homozygous lines in potatoes makes genemapping and breeding a very slow and challenging process.

The potato genome sequencing was projected to be completed within 6months bythe international Potato Genome Sequencing Consortium (PGSC). The completionof the genome sequence will no doubt provide valuable information about thegenome arrangement, diversity, functional genes, and gene alleles. Major potatogenome databases available are PGSC (www.potatogenome.net), The Institute forGenomic Research (TIGR) Solanaceae Genomics Resource (http://jcvi.org/potato),The Canadian Potato Genome Project (www.cpgp.ca), Solanaceae CoordinatedAgricultural Project (http://solcap.msu.edu), and theDFCI Solanum tuberosumGeneIndex (StGI) (http://compbio.dfci.harvard.edu/tgi/cgi-bin/tgi/gimain.pl?gudb¼potato). Many functional genomics studies have already used the sequencinginformation for trait analysis and marker discovery. Over the past 10 years, thepotato research community around the world has also established extensive genomic

1122j 44 Potato: Improving Crop Productivity and Abiotic Stress Tolerance

resources, including expressed sequence tag (EST) libraries, SAGE libraries, micro-arrays, molecular function maps, and mutant populations [1–3]. Genomic data fromEST libraries, molecular linkage maps, andmicroarray expression analyses will helpidentify the genetic components underlying many of the traits, for example, yield,quality, and abiotic and biotic stress managements. In addition, natural geneticresources (wild potato varieties and germplasm collections) can be used in concertwith genomic tools such as marker-assisted selection, polymorphism identification,and association mapping to improve breeding lines.

44.3Abiotic Stresses Related to Potato Production

Potatoes grow the best under long and hot day and cool night conditions. They arevery sensitive to light, water, and sources of nitrogen. Any stress condition, such aswater, temperature, salinity, or mechanical damage, will significantly impact theyield, tuber quality, andmarketing value. Even a short period of acute stress can causea substantial decrease in total andmarketable yield. For the North Americanmarket,50% of the potatoes are processed during storage, so postharvest stress to tubers canfurther reduce the marketable quality and produce low temperature-induced coldsweetening and after-cooking darkening (ACD), disorders that are induced orexacerbated by storage conditions.

This chapterwill focus onfive key abiotic stress issues: drought, heat, cold and frost,salinity, andwounding. Since themolecular basis for the stress responses is the key tounderstanding the stress management mechanisms in potatoes, we have providedinformation about cellular responses and regulation of each stress, and then providedan overview on the research outcomes inmolecular gene functions and omics studies.Owing to the large volume of literature for these topics in potatoes, we did not compilean exhaustive list of references, but rather included those that highlight key findingsand employ an �omics� perspective to provide insight to direct future work.

44.3.1Water and Drought Stress

Water is becoming an increasingly scarce resource on earth. Approximately, 80countries with 40% of the world population suffer from serious water shortage. Thepotato produces more food energy per unit water on dry weight basis than the otherfood crops [4]. Thus, water productivity in potatoes is two to three times higher thanthat of maize, rice, and wheat [5]. Ironically, although the potato crop uses waterrelatively efficiently, it is also characterized as more drought sensitive than otheragronomic crops. This is, in part, due to a lower root length density compared to theother crops. Therefore, in the low rainfall areas, utilization of irrigation systems is notuncommon if higher yield and quality are desired. Drought tolerance ismeasured bythe relative ability of a variety to produce tubers from a limited amount of water [6].However, water requirements vary for different stages of plant development (shoot

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and stem growth, and tuber formation) and tuber bulking,making the entire processdifficult to control and predict. Studies normally look into early drought or latedrought conditions. If the drought conditions appear early in the season, the plant�ssurvival strategy is tominimizewater losses to transpiration; thus, leaf growth beginsto slow down, followed by reducing areal growth and canopy size [7]. If the conditionsdo not improve, the plants will have a reduced capacity for light interception,resulting in lower yields [8].

In potato production, varieties are often categorized by early or latematuring. Thismakes the situation even more difficult to manage. Some early-maturing potatovarieties escape late-season drought events, whereas late-season drought maysignificantly impact yield losses in late-maturing varieties [9]. There is a varietydifference in drought tolerance in potatoes and the effect of drought timing alsodepends on genotype. For some varieties, the effect is more profound when droughtoccurs during tuber initiation [10–12], while in others more critical during tuberbulking period [13, 14].

44.3.1.1 Effect of Drought on Tuber QualityDrought has significant impact on a variety of tuber qualities and defects. Droughtcan cause tuber cracking, secondary growth, malformations, hollow heart, andinternal brown spot. Drought can adversely increase the contents of glycoalkaloidssuch as a-solanine and a-chaconine, compounds that are believed to cause cancerand other health problems. Drought can also cause sugar end, a disorder charac-terized by relatively low starch and high sugar content in the basal end of the tuber.Processing these tubers resulted in French fries with dark and discolored ends.Stressed plants accumulate large amounts of sucrose in the basal tissues of the tuberimmediately following stress. This is because water deficit, as well as heat stress,induces changes in the activities of certain key carbohydrate metabolizing enzymes,shifting the tuber from a starch synthesizing function to starch mobilization.Drought-stressed plants are also more susceptible to biotic stresses; for example,drought conditions increase pest disease infestations of cyst nematodes [15, 16]and drought reduces transpiration and stomatal conductance, which increasesVerticillium-related wilting disease.

44.3.1.2 Drought Sensing MechanismsRoot drymass was found to be critical for water stress conditions, as it is significantlycorrelated with leaf area, photosynthesis, reduction of stomatal conductance, andtuber yield [17]. If drought occurs before tuberization, the plants will lose the ability toproduce a higher number of stolons per stem [18], resulting in a lower tuber yield. If itis during tuber bulking stage, it will lower both tuber number and size [19]. It isunderstood that plant responses to drought, including stomatal reactions, aretriggered by root signals, not just leaf water potential. In this case, abscisic acid(ABA) plays an essential role in stress signaling. At least four independent regulatorysystems for gene expression changes in response towater stress have been identified,two are ABA dependent and two are ABA independent [20]. When potato roots sensesoil water deficits, well before leaf water potential drops, ABA is produced in root tips


and transported through the xylem to the leaves to attenuate growth and closestomata [21]. Such signal transduction pathways include a plethora of secondarymessengers such as hormones, phospholipids, and calcium ions [22].

Decreased accumulation of reactive oxygen species (ROS), greater mitochondrialactivity, and active chloroplast defenses all contributed to themanagement of droughtstress in a drought-resistant cultivar. In stressed plants, the primary sources of ROSare the Mehler reaction and the antenna pigments in the chloroplasts, the photo-respiratory pathway in peroxisomes, the cytochrome reactions in the endoplasmicreticulum and cytoplasm, and oxidative processes in the mitochondria. Underdrought conditions, drought-tolerant potato lines upregulated members of all majorROS scavenging enzymes in the chloroplasts: superoxide dismutase (SOD), ascor-bate peroxidase (APX), catalase (CAT), glutathione peroxidase, and peroxiredoxingene families [23–26]. In addition, other genes encoding proteins that contribute toincreased ROS scavenging capacity such as glutathione synthetase, glutathione-S-transferase, glutathione transporter, two thioredoxins, and four thioredoxin-relatedchloroplast-targeted genes were induced in a drought-resistant accession [24, 27].Evidence also showed that several genes in the biosynthesis pathway of antioxidantcompounds, such as flavonoids, anthocyanins, and xanthophylls, were stronglyinduced in tolerant cultivars. In another study, gene transcripts of three key enzymesin the biosynthesis of flavonoid and carotenoids were increased in leaves and rootsunder mild and moderate drought conditions [28].

Osmotic adjustment is the process by which plant cells maintain turgor duringwater deficit. The osmotic potential inside the cytoplasm is lowered by the accumu-lation of osmolytes (also called compatible solutes) such as amino acids andsugars [29]. Proline and trigonelline are two compounds that have received a lotof attention as potential compatible solutes and it has been suggested that prolinecould act as an antioxidant [30]. The accumulation of these compounds is oftenobserved in response to hyperosmotic stress [31, 32] and in response to a combinedtreatment of heat and drought stress [33, 34]. In one study, drought caused anincrease in proline, trigonelline, and proline analogues in a drought-resistant potatocultivar, whereas the drought-susceptible cultivar had an increase only in prolineanalogues [35]. In another study, proline increased in both drought-resistant and-susceptible potato cultivars [24]. Nevertheless, the role of proline remains contro-versial. Proline levels often increase earlier in drought-susceptible varieties than inmore tolerant ones, which has led to the conclusion that proline is only an indicator ofplant water status but not of tolerance. Others have suggested that because minorproline analogues, such as hydroxyproline, increase during drought stress, they mayplay a role in increased synthesis or reconstitution of cell wall components [36], andthere is someevidence that free proline synthesized in other plant parts is transportedto the roots to be used for cell wall synthesis in the apical region [37].

44.3.1.3 Breeding through Omics ApproachesTraditional breeding has made limited success in drought tolerance using existingpotato germplasm. This is partly because the timing and severity of naturallyoccurring drought is quite erratic and so plants tend to respond differently from


year to year. As a result, the early stages of breeding programs often aim for highyield in favorable environments, but these gains are not usually maintained inenvironments commonly affected by severe stress. In addition, direct selection fordrought tolerance under water-stressed conditions is hampered by low heritability,polygenic control, and epistasis of many drought tolerance traits [27]. Anotherobstacle for breeding programs is a reluctance to use unadapted parents, such as awild potato species. It is also difficult to breed for tropical environments wherehigh temperatures are a factor because many drought tolerance traits might not beeffective when the plant experiences a combination of both drought and heateffects.

44.3.1.4 Pathways Involved in Drought StressComparing transcriptomic and metabolomic profiles of tolerant and susceptiblegenotypes has led to the identification of some changes in photosynthesis and carbonand amino acid metabolism that are closely related to drought tolerance [35]. It wasalso found that drought stress regulates osmotic adjustment, carbohydrate metab-olism, membrane modifications, strengthening of cuticle and cell rescue mechan-isms, detoxification of oxygen radicals, and protein stabilization [24]. In addition,drought stress increases ethylene biosynthesis thatmay subsequently increase stressperception since ethylene and ABA attenuate leaf growth under water stress [24, 38].Drought treatment also induces a number of ABA-responsive genes and leads to anaccumulation of gibberellins degrading enzymes.

Stomatal closure under drought conditions prevents CO2 supply for photosyn-thesis, leading to a reduction in net photosynthesis. This repression triggersregulation of genes functioning in the light reaction, Calvin cycle, and chlorophyllbiosynthesis [35] and is accompanied by an increased expression of genes related tophotorespiration and cyclic electron transport in photosystem I [24, 35]. Somedrought-resistant genotypes, presumably under tolerable drought conditions, upre-gulated photosynthesis-related genes, while the same genes are downregulated indrought-susceptible genotypes [39].

Drought stress also represses transcription of genes involved in carbohydratebiosynthesis, glycolysis, and the tricarboxylic acid cycle, while sucrose metabolismis induced. These changes are required because under drought conditions,carbohydrate metabolism is redirected to reserve mobilization, as illustrated byinduction of starch degrading enzymes, invertase and sucrose synthase [23, 24].This was proved by Watkinson�s study [40] in which expression profiles of genesassociated with carbon metabolism contributed to differences in tuber develop-ment in phenotypes of adapted and acclimated, drought-stressed S. tuberosum ssp.andigena.

Finally, attention needs to be given to genotype differences in stress responsestrategies.Mane et al. [23] analyzed two potato landraces during drought and droughtrecovery. One landrace, Sullu, maintained vegetative biomass accumulation duringdrought while the other, Ccompis, experienced reduction in vegetative growth.Interestingly enough, both landraces maintained the same tuber yields as non-stressed controls. In Sullu, themain response that helpedmaintain vegetative growth


appears to be a capacity to uphold photosynthetic efficiency, minimize stomatalresistance, and activate photosynthetic genes during recovery. Other differences thatare perhaps caused by the increased photosynthetic capacity include increased cellwall biosynthesis, maintenance of plastid SOD transcripts, and significant increasesin sucrose, trehalose, and proline. By contrast, Ccompis differs in all of these aspects,most importantly in respect to photosynthesis. This study demonstrates that adiversity of effective strategies for dealing with abiotic stresses may exist naturallywithin the potato germplasm.

44.3.1.5 Genes Involved in Drought Stress SignalingMany genes have been identified and their functional studies have shown promiseswith regard to drought tolerance. Transcriptomic studies found upregulation ofgenes for Ca2þ binding and GTP binding factors, kinases, and phosphatases [24].Genes encoding several protein phosphatases 2C (PP2C), negative regulators of ABAsignaling in Arabidopsis, are potential candidates for yield maintenance underdrought conditions [41, 42]. Drought stress induced nitrite reductase and a chloro-plast PII nitrogen-sensing protein, known to activate glutamine synthase [43].Cysteine biosynthesis and sulfur uptake genes, such as adenosine phosphosulfatereductase, are upregulated at an early stage of drought condition, but reversed torepression under prolonged drought [35].

Transcription factors are actively involved in drought stress response. Both ATHB-7 and RD26 are upregulated by drought and function in one of the ABA-dependentregulatory systems, whereas a dehydration-responsive element DREB is regulated inABA-independent regulatory systems [39]. Two other factors, ASR1 and ASR2, arestrongly upregulated by drought stress [24]. ASR1, when present in the nucleus,regulates the expression of a hexose transporter, while in the cytosol, it functions as achaperone to stabilize proteins under abiotic stress conditions [44]. Other transcrip-tional factors found aremembers of theWRKY, SCARECROW,MYB, CCR-4, TAF-3,and NAM transcription factor families. They are commonly induced by elevatedH2O2 levels in potato leaves under drought conditions [24].

Polyols are osmotically active solutes that can effectively replace water in establish-ing hydrogen bonds and thereby protect enzyme activities and membranesexperiencing water stress [45]. Drought-stressed cv. Sullu had both increased levelsof a polyol (galactinol) and its precursors (galactose and inositol) and increasedtranscript levels of two genes (glucose-4-epimerase and galactinol synthase) involvedin galactinol synthesis [35], whose overexpression in Arabidopsis thaliana has beenshown to increase drought tolerance [46, 47]. Transgenic potato lines of cv. Desireethat overexpressed a dehydrin 4 (DHN4) isolated from barley, or a stress-inducible,heat-stable LEA group 3-like protein from bromegrass (ROB5), showed significantpotential to enhance yield under moisture stress [48]. Interestingly, a wild tuber-bearing species, Solanum gandarillasii Cardenas, was found to exhibit reducedosmotic adjustment responses resulting in low transpiration rates [49].

Membranes are the main targets of degenerating processes caused by drought.During drought stress, there is a significant upregulation of nonspecific lipid transferprotein genes [50]. Other drought stress-induced gene products, such as heat shock


proteins (HSPs) and chaperones are used to protect cellular structures by maintain-ing the hydration of cellular compounds such as proteins and membranes. Oneorthologue to the Arabidopsis HSP At5g12030 was found to enhance droughttolerance [51]. An HSP DnaJ gene family was found to increase drought tolerancein potatoes [24, 25]. Others reported that an ATP-dependent metalloprotease andchaperone are induced in potatoes for drought tolerance [52].

44.3.1.6 Gene Testing in Transgenic LinesMany labs have employed a transgenic approach to test candidate genes for improveddrought tolerance in potatoes. Waterer et al. [48] tested the functions of constitutiveCaMV 35S promoter or a stress-induced Arabidopsis COR78 promoter for theoverexpression of four transgenes. The transgenic lines with the COR78 promoterproduced higher yield under nonstressed conditions than the 35S promoter [48].Interestingly enough,most of the transgenic lines demonstrated higher yields underdrought stress in field trials. As plants respond to many stresses using similarmechanisms, Tian et al. [53] studied the potato zinc finger protein StZFP1 that isinduced by salt and exogenous ABA. Findings are worth to explore further forstudying stress management in plants. Transgenic potatoes expressing trehalose-6-phosphate synthase (TPS1) had a 30–40% reduction in stomatal densities. Thisappeared to cause lower CO2 fixation rates under normal and drought-stressedconditions, enabling TPS1 plants to conserve water [54].

Transgenics overexpressing genes encoding antioxidant enzymes improved thedrought tolerance of potatoes. Overexpression of nucleoside dikinase 2, Cu/Zn-SOD,and APX improves drought tolerance [55–57]. Transgenic potato lines of cv. Desireethat overexpressed wheat mitochondrial MnSOD3:1 under the direction of a stress-inducible COR78 promoter showed significant potential to enhance yields undermoisture stress [48]. Simultaneous expression of choline oxidase, superoxide dismu-tase, and APX in the potato chloroplasts provides synergistically enhanced protectionagainst salt and drought stresses at the whole-plant level [58]. Transgenic potatoesoverexpressingArabidopsis glutathione reductase gene (AtGR1) exhibited faster recov-ery fromdrought andwith less visual injury compared tonontransformedcontrols [59].Higher percentages of the reduced ascorbate were observed for transgenic potato andpoplar trees with overexpressed glutathione reductase [60], which might be attributedto thehigherglutathione levels in the transgenicplants [59]. Another study showed thatoverexpression of both Cu/Zn-SOD and APX genes in sweet potato (Ipomoea batatas)leaves can protect them fromstress environment and enhance their drought tolerance.Finally, it was found that genes related to the accumulation of ROS could improvedrought, salinity, and oxidative stress tolerance [61].

44.4Heat Stress and Thermotolerance

Temperature during the growing season affects the dynamics of the growth anddevelopment of the potato plants, resulting in the significant effects on yield and


quality of potato tubers. For a complete coverage of the issue, read the compre-hensive review given by Struik [62]. As Striuk pointed out, it is important to note theparts of the plants that are exposed to certain temperatures and the period ofexposure to specific temperature treatments. In this review, estimated optimaltemperatures for each stage of the plant cycle are given. Temperatures significantlyhigher or lower than the optimal levels will cause stress to the plants or can damagethe plant or tubers during growth and storage. Heat injury and sunscald are thedamages to foliage and tubers caused by high temperature (>25 �C) and/or directsunlight. Most of the leaf injury occurs during intense dry weather and when thereis a strong wind (air temperature >30 �C). Tubers lying in the collection rows afterdigging may be injured internally or externally when exposed to direct solarradiation and high temperatures.

Recent attention on global warming should bring some concerns on potatoproduction. Projections indicate that global average temperatures will increase from1.1 to 6.4 �C by the end of this century, depending upon region [63]. Generally,increasing CO2 concentrations and air temperatures will result in lower growth andyield, reductions in the duration of the plant cycle and increase in potato diseases.Thus, the development of cultivars that are tolerant to high temperatures is critical tothe strategy to minimize the global warming effects. Furthermore, the problem iscompounded when other stresses, such as drought and salt, are factored in. Forexample, somewild Solanum species effectively deal with drought stress by reducingtranspiration rates; however, this also reduces evaporative cooling effects that in turnrequire leaves to possess a higher thermal tolerance [49]. If heat stress is added to saltstress 40–60 days after emergence, the mechanisms that normally prevent saltaccumulation fail and the young expanding leaves can be permanently damaged.

A number of tools including cultural practices and genetics are available toameliorate heat stress. It appears that potato leaves grown under heat stress exhibitimpaired cell expansion, but this can be overcome by increasing root zone calciumlevels to promote axillary shoot growth [64]. Literature has suggested a significantamount of variation in tolerance to heat and cold stresses both among S. tuberosumcultivars and wild relatives [23, 49, 65–69]. These variations may provide breedingmaterials to develop thermotolerant varieties.

44.4.1Effect of Heat on Tuber Quality

Heat stress andwater deficit appear to induce changes in carbohydratemetabolism inthe tuber, shifting from starch synthesis to starch mobilization [70]. The frequencyand severity of internal heat necrosis, a disorder that manifests in the form of brownspots in the tuber flesh, affects fresh market and processing quality. Such defectoccurs when the early growing season is subjected to high day and night tempera-tures and low rainfall [71]. The same weather conditions can also cause sugar end,which results in dark coloredFrench fries. In addition, skin russeting occurs in potatotubers exposed to high soil temperatures, which triggers the production of thick andprotective skin layers that become cracked with subsequent tuber expansion [72].

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44.4.2Cellular Response to Heat

Heat as a signal triggers several plant responses, including production of HSPs,molecular chaperones, osmoprotectants, and oxidative response pathways. Thesemolecules protect macromolecular structures and proteins from denaturationduring heat stresses. For example, stress-induced tomato ABA stress ripening 1(SIASR1) protein has chaperone-like activity and can stabilize a number of proteinsagainst denaturation caused by heat and freeze–thaw cycles [44]. The heat-tolerantpotato cultivar Norchip, when exposed to high temperatures (40 �C), synthesizedsmall HSPs for a longer time period than other more heat-sensitive cultivars [69].Oxidative stress also plays a role in heat stress. For example, a sweet potatoperoxidase (SWPA4) responds to several abiotic stresses and contains a cis-actingheat shock element in its promoter [73]. Tang et al. [56, 74] developed several potatolines using an oxidative stress-inducible SWPA2 promoter to express either Cu/ZnSOD and APX in the chloroplasts or Arabidopsis nucleoside diphosphate kinase 2(NDPK2) in the cytosol. In both cases, the presence of the transgene greatlydiminished the reduction in photosynthetic activity that was caused by hightemperatures (42 �C for 20 h) [56, 74]. In another study, Waterer et al. [48] trans-formed cultivar Desiree to overexpress one of the four genes: mitochondrialMnSOD3:1 from wheat or a cold-inducible transcriptional factor DREB/CBF1from canola, as well as the two previously mentioned genes encoding dehydrin 4(DHN4) from barley and LEA group 3-like (ROB5) from bromegrass [48]. All of thetransgenes appeared to enhance the heat stress tolerance (44 �C) of whole plants orexcised leaves, with lines transformed with SOD3.1 showing the greatest effect. Inlow-temperature stress trials conducted under controlled environment and in thefield, lines overexpressing SOD3:1 showed an enhanced capacity to grow atsuboptimal temperatures (10 �C), while lines transformed with SOD3.1 or ROB5had greater tolerance to freezing temperatures than the parental lines [48]. There-fore, there may well be similar cellular mechanisms in potatoes when dealing withhigh or low temperature stresses.

44.4.3Cultivar Development through Omics Approaches

Few studies have been completed at the omics levels. Below are the three individualstudies that have provided some key information about the pathways that areregulated by heat, cold, and salt. Readers should by now realize that cells use similarmechanisms to respond to different stresses, that is why often similar genes andpathways are foundunder different stress stimuli. Rensink et al. [75] generated 20 756ESTs from a cDNA library constructed by pooling mRNA from heat, cold, salt, anddrought-stressed potato leaves and roots and termed it the potato abiotic stress (POA)collection. This collection contained 1476 unique sequences, 667 contigs, and 809singleton ESTs. In their subsequent study [76], researchers used a �12 000 clone


potato cDNA microarray to measure the expression of seedlings grown undercontrolled conditions and subjected to cold (4 �C), heat (35 �C), or salt (100mMNaCl) stress for up to 27 h. They discovered that potato gene products implicated instress adaptation were similar to those reported in other plant species, such asmolecular chaperones, HSPs, late-embryogenesis abundant proteins, and geneproducts with enzymatic activity, as well as several transcription factors, signaltransduction proteins, and hormone signaling-related genes. In a study that focusedon skin russeting induced by heat stress, Ginzberg et al. [72] looked into thetranscriptomic profile of the periderm of tubers. Results revealed the upregulationof genes encoding heat shock proteins and regulation of transcription factors andgenes related to cell proliferation and differentiation.

44.5Cold and Frost Stresses

Potato plants can be injured by low temperature and frost in the field during thegrowing season. Low-temperature injury occurs when the leaf temperature dropsbelow 0 �C, but tissues are not yet frozen. Frost damage occurs when the leaf tissuesbecome frozen. At the end of the growing season, tubers in the ground can be injuredby cold and frost. They become very sensitive to mechanical damages due to lifting,transport, and storage. Potato tubers can be damaged when the temperature is below3 �C. The severity of the damage depends on variety, temperature, and the exposureduration.When the storage temperature is between freezing and 9 �C, tuber starch isconverted into sugar, resulting in cold sweetening. Cold sweetening is a majorprocessing defect, causing brown color after frying for French fries and chips. Whenthe temperature is below 3 �C, tubers can be damaged internally and externally. Thedamaged tissues will rot by bacterial pathogens soon after.

Cold conditions that could cause damage to potatoes are temperatures belowwhichcells can handle for normal physiological activities. For clarity in this section, we willuse the terms cold tolerance and cold acclimation to refer to low temperatures abovefreezing, and we will use freezing tolerance to refer to temperatures below 0 �C.While cultivated potato (S. tuberosum) doesnot have the ability to cold acclimate, somewild Solanum species can be acclimated to cold by exposure to low temperature(�4 �C) for a period of time [77]. The degree of cold acclimation can be assessed byseveral methods including visual inspection or by measuring changes in electricalconductivity of the leaves and estimated by the LT50 corresponding to the temper-ature inducing 50% of injured cells [77]. There is a quite overlap among differentstress responses. For example, microarray analysis indicates that leaves respond tocold and salt stresses very similarly at 9 and 27 h [76].

In response to low-temperature stress, plant membrane lipids have a tendency tochange from gel to liquid-crystalline phase due to the increased level of lipiddesaturation. Thus, fatty acid desaturases have been the focus of improving coldtolerance in plants [78]. It has been found that an increase in 18 : 2 (linoleate) in the

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purified plasma membrane fraction during cold acclimation is associated withgenetic variations in cold acclimation capacity [79]. This increase was found onlyin genotypes that are able to cold acclimate and was reversible on deacclimation,suggesting a link between the accumulation of 18 : 2 and the acquisition of freezingtolerance [80]. An accumulation of D9 desaturase gene transcripts during coldacclimation is confirmed to be associated with the cold acclimation response inpotatoes [80]. Also, cold tolerance (long-term growing at 8 �C), as well as freezingtolerance (�7 �C for 30min), was enhanced in transgenic lines expressing an acyl-lipidD12-desaturase gene from Synechocystis spp. PCC6803 because of an increasedunsaturated fatty acid concentration in their lipids, with increased content of 18 : 2and 18 : 3 fatty acids [81, 82].

Lipid profile is, therefore, an effective measure of the cellular responses to coldstress. One study compared the lipid profiles between a freezing-tolerant, cold-acclimating wild potato species (S. commersonii) and a freezing-sensitive, nonaccli-mating cultivated species (S. tuberosum). Following cold acclimation, both specieshad a decrease in palmitic acid, an increase in unsaturated to saturated fatty acid ratio,an increase in free sterols, an increase in sitosterol, and a slight decrease incerebrosides. Lipid changes detected only in the acclimating species included anincrease in phosphatidylethanolamine, a decrease in sterol to phospholipid ratio, anincrease in linoleic acid, a decrease in linolenic acid, and an increase in acylated sterylglycoside to steryl glycoside ratio [83]. This study highlighted the importance ofmembrane lipid profiles in regulating frost and cold tolerance in plants. Anotherstudy [84] has shown that during low-temperature treatment, Solanum species thatare able to acclimate to cold induced a noticeable increase in SsLTP1 (a lipid transferprotein), while species that display a low capacity for cold acclimation had no changein SsLTP1 levels.

44.5.1Cellular Response to Cold

In response to cold stress, cells accumulate osmoprotectants, small molecules thatbalance the osmotic difference between the cell surroundings and the cytosol.Upon cold exposure, carbohydrates accumulated in cultivars that are cold toler-ant [77]. It is worth to point out that even under nonstressed conditions, mostcarbohydrates (sucrose, galactose, galactinol, raffinose, and glucose) were presentat higher levels in the constitutively tolerant cultivar S. phureja. In this plant,trehalose levels reached concentrations equal to those of other carbohydrates,giving evidence that the sugar acts as an osmoprotectant rather thanmerely playinga regulatory function as has been suggested in other situations [85]. Expression ofcarbohydrate-related genes during cold exposurematches thesemetabolite profilesin cultivar Desiree, showing the upregulation of sucrose synthase and galactinolsynthase, leading to galactinol and eventually raffinose accumulation [77]. Freepolyamine accumulation has been demonstrated to be involved in abiotic stresstolerance in other species [86, 87]. This was also detected in potatoes where freepolyamine metabolism was affected by cold as shown through an upregulation of


arginine decarboxylase, S-adenosylmethionine decarboxylase, and spermidinesynthase genes [77, 88]. Potato plants transformed with an apoplastic-localizedyeast invertase had a greater invertase activity, higher content of sugar, andproduced significantly less lipid peroxidation activity when exposed to low tem-perature (3 �C) and freezing temperatures (�1 or �9 �C) [89, 90]. The authorssuggested that the improved cold tolerance was attributed to the stabilizing effect ofsugar on the membranes.

Cell signaling is one of the most important cellular responses to cold treatment.Potatoes possess at least three calcium/calmodulin signaling proteins that displaydifferential expression in response to cold stress in leaves after cold acclimation, andwhen combined with osmotic stresses [91]. Plant hormones, such as ABA pretreat-ment confers freezing tolerance tomicroplants transferred to soil, with no significantnegative long-term effects on tuber production. Responses to ABA were found to beassociatedwith increased antioxidant enzymatic activities of peroxidase andAPX anddecreased H2O2 content in the induction of freezing tolerance in the potato [92].Antistress effects of salicylates can also be used in a planned manner to improve invitro culture technology and hardening in potatoes for induction of tolerance tofreezing in microplants after transplanting them to soil [93]. It appears that at leasttwo mechanisms are involved in the induction of freezing tolerance in potato bysalicylic acid (SA). One mechanism, exemplified in the cold-sensitive cultivarAtlantic, appears to involve induction of hydrogen peroxide (H2O2) accumulationleading to enhanced CAT activities, while another mechanism exemplified in themore cold-tolerant cultivar Alpha does not appear to involve H2O2 accumulation orenhanced CAT activities [94].

ROS generated during cold stress are involved in inducing the oxidative stressduring chilling and in triggering cold-induced damage [95]. ROS can either act assignals that induce protection mechanisms or accelerate injury [96]. Freezingtolerance is attributed to the protective effect of sugars caused by their ability toscavenge ROS nonspecifically under stress conditions [97, 98].

44.5.2Gene Functions and Omics

Protective proteins are produced under cold stress conditions. Pruvot et al. [99]identified CDSP34 protein that accumulates in the chloroplast in response to lowtemperatures. This protein plays a role in the structural mechanisms involved in thethylakoid tolerance to stress. A chaperonin protein Cpn60b involved in sustainingproper protein folding under stress was found to be constitutively expressed at ahigher level in cold-tolerant potato species S. commersonii, but not in cold-susceptibleS. tuberosum [100]. Dehydrins are believed to act as emulsifiers or chaperones in thecells by protecting proteins and membranes against unfavorable structural changescaused by dehydration. One of the dehydrin proteins, dhn2, was found to express at ahigher level in cold-tolerant potato species [100]. Furthermore, the cold acclimationthat improved the freezing tolerance in S. commersonii was associated with theaccumulation of the transcripts of Scdhn2 [96]. A similar response to cold acclimation


was also observed for DHN24 (a SK3-type dehydrin protein) [101] and TAS14 [88]. Asmentioned previously, overexpression of DHN4 in potatoes did not provide anybenefit with respect to cold tolerance, although in the same trials, overexpression ofmitochondrial MnSOD3:1 did confer tolerance [48].

In low-temperature stress trials conducted under controlled environment and inthe field, lines overexpressing a heat-stable, LEA group 3-like protein from brome-grass (ROB5) had greater tolerance to freezing temperatures than the parentalline [48]. Another class of proteins commonly studied in relation to cold and freezingtolerance are antifreeze proteins (AFPs) that inhibit ice growth and recrystallization.Expression of a synthetic AFP (similar to type 1 AFP of winter flounder) in cultivarRusset Burbank conferred freezing tolerance as assessed by electrolyte releaseanalysis of the transgenic plant [102].

Many transcription factors regulate gene expression under cold conditions.Transgenics overexpressing several transcription factors (ERF, EREBP, DREB, andCBF) have improved freezing tolerance in potato plants. Ethylene-responsive factors(ERFs) are plant-specific transcription factors, many of which have been linked toplant defense responses. Overexpression of CaPF1, an ERF/AP2-type pepper tran-scription factor gene, effectively increased tolerance to freezing in potatoes [103]. Inaddition, StEREBP1 (ethylene-responsive element binding protein 1) is a transcrip-tion factor that responds to several environmental stresses. Overexpression ofStEREBP1 enhanced tolerance to cold stress (growth at 8–10 �C for 2 months) intransgenic potato plants [104]. Overexpression of Arabidopsis rd29A::DREB1A alsoenhances freezing tolerance in transgenic potatoes [105]. Even in the absence of coldtreatment, ectopic AtCBF overexpression improved the freezing tolerance of trans-genic Solanum species [106]. In the meantime, overexpression of ectopic AtCBF1affected many alterations associated with cold acclimation such as thickening ofleaves and increase in proline and total sugar contents. The leaves of these transgenicS. commersonii were darker green, had higher chlorophyll and lower anthocyaninlevels, had greater stomatal numbers, and displayed greater photosynthetic capacity,suggesting their higher productivity potential [107].

It is worth mentioning several other genes. For instance, potato 1-aminocyclo-propane-1-carboxylate oxidase genes, ACO1 andACO2, can be induced by cold stress(0 �C), but are differentially expressed by other stresses such as heat, wounding, andsoil flooding [108]. Renaut [109] presented a series of studies on the cold response intwo genotypes of S. tuberosum, PS3 and Desiree. Oufir et al. [77] focused oncarbohydrates and polyamines because they are known cryoprotectants associatedwith cold acclimation. They used transcriptomics and metabolomics approaches todemonstrate how three genotypes of potato responded to chilling exposure: atetraploid S. tuberosum (cultivar Desiree) was not able to acclimate to cold, a dihaploidS. tuberosum (PS3) acclimated to cold, and S. phureja (CHS) wasmore tolerant to coldon a constitutive level. Although free polyamine accumulation was not pronouncedupon cold exposure, an array of genes involved in several other metabolisms, forexample, amino acid, carbohydrate, energy, detoxification, and photosynthesis, weredifferentially expressed in these potatoes under cold exposure.


44.5.3Cold-Induced Sweetening during Storage

Refrigeration is the most important and effective technology employed to maintainthe postharvest quality of potatoes. Storage at cold temperatures prevents sprouting,minimizes disease losses, reduces shrinkage, and improves the retention of drymatter and extends the marketability, thus supplying consumers and the processingindustry with high-quality tubers throughout the year. Unfortunately, when tubersare stored at temperatures between 2 and 4 �C, they undergo a phenomenon knownas cold sweetening or low-temperature sweetening (LTS). At these temperatures, therate of conversion of starch to reducing sugars (i.e., glucose and fructose) isaccelerated. These potatoes are unacceptable for processing into chips or Frenchfries because when cooked in oil at high temperatures, the accumulated reducingsugars react with free amino acids in the potato cells, forming a brown toblack pigmented and bitter-tasting product via a nonenzymatic, Maillard-type reac-tion [110, 111]. Such products also have elevated amounts of acrylamide, a neurotoxinand potential carcinogen [111]. Therefore, LTS is a major concern since all com-mercial potato cultivars used for the production of potato chips and fries accumulateexcess free reducing sugars when exposed to cold stress.

The mechanism of LTS is somewhat understood. Low-temperature storage ofpotato tubers induces amylolytic enzymes that initiate the breakdown of starch storedin the amyloplasts. The breakdown products, both hexose phosphates (hexose-P) andfree sugars, are exported from the amyloplast to the cytosol where they are convertedto sucrose [112]. Sucrose-phosphate synthase produces sucrose 6-phosphate (Suc6P)andUDP fromUDP-glucose and D-fructose 6-phosphate. Then, Suc6P is hydrolyzedby sucrose phosphatase (SPP) to yield sucrose and inorganic phosphate (Pi) [113].This sucrose can then be hydrolyzed into its constituent hexoses by soluble acidinvertase [114].

A genomic investigation by the Canadian Potato Genome Project initiative (www.cpgp.ca) [115] sheds some light on LTS. In this study, mature, harvested tubers ofcultivar Shepody were stored at 4 �C for 3 months. Normalized library was con-structed and ESTs were sequenced. Among the 5000 ESTs identified, only 7transmembrane proteins Mlo8 and putative protein transport protein SEC13 werehighly regarded, while others were marked unknown. With the complete genomesequencing data like to soon become available, these genes could be revisited for theirfunctions related to LTS.

At present, sucrose phosphatase and the vacuolar acid invertase (VInv) are targetedin order to control LTS. Chen et al. [116] suppressed sucrose synthesis by RNAi-mediated silencing of SPP expression, leading to an accumulation of Suc6P. Overall,SPP-silenced tubers exhibited only minor differences in total soluble carbohydrateaccumulation. However, the sucrose to hexose conversion was greatly reducedbecause of an unexpected blocking of cold-induced expression of VInv. Bhaskaret al. [111] used a targeted RNAi approach to demonstrate that the potato VInv isresponsible for reducing sugar accumulation in cold-stored tubers. Evenwhen tubers


were stored at 4 �C, potato chips processed from VInv-silencing lines were light incolor and showed a 15-fold reduction in acrylamide [111]. In a more traditionalbreeding approach, Hamernik et al. [117] achieved a similar goal by introgressingwild species germplasm with extreme resistance to cold sweetening at very lowstorage temperatures (2 �C) into the cultivated potato. Selected accessions werecrossed as males to haploids of S. tuberosum to produce adapted hybrids, whichproduced good tuber type and low levels of reducing sugars under extremely lowstorage temperatures [117]. Interestingly, comparable low levels of VInv geneexpression were observed in cold-stored tubers of VInv silencing lines and wildpotato germplasm stocks that are resistant to cold-induced sweetening. These resultsdemonstrate that both processing quality and acrylamide problems in potato can becontrolled effectively by suppression of the VInv gene through biotechnology ortargeted breeding.

Several other attempts had been made to control LTS, by manipulating VInvactivity through the ectopic expression of an invertase inhibitor [118–120], throughantisense inhibition [114], or through RNAi suppression [121, 122]. The success ofthese efforts was limited because invertase activity was only partially reduced. Itseems a nearly complete silencing of the VInv gene is required to effectively controlLTS [111].

44.6Salt Tolerance

Soil salinity is defined as excess sodium chloride (NaCl) in soil. Plants encounter saltstress when grown in naturally occurring saline soils or when irrigated with salinewater. According to the review by Donnelly et al. [123], most of the areas in the worldunder potato cultivation are in countries that are not overly affected by salinity. Theexceptions, as pointed out by the authors, are countries in Southern andSoutheasternAsia. Since China and India have become the top two potato producers in the world(producing over 30% of the world potatoes), the salinity problem could become amajor issue for these two countries. In order to maintain production levels in thesecountries, potato cultivars with improved stress tolerance to heat, drought, andsalinity are the top priority.

Irrigation has become an important agricultural practice, which is employed toproduce up to 30% of the world�s food using 15% of the cultivated land area. Saltinjury occurs when high-concentration salt water comes in contact with above- orunderground plant parts. This contact will lead to withdrawal of water from the planttissues due to osmotic pressure. The injured tissue cannot resume normal functionsand lead to necrosis.

Mechanisms of salinity tolerance in plants are related to a combination of plantstresses, including drought stress, ion toxicity, mineral deficiency, and oxidativestress. Because salinity affects major biochemical processes of the cell, such asprotein synthesis, energy generation, photosynthesis, and lipid metabolism, plantsuse diversified mechanisms to counter these effects. These include limiting the


uptake and transport of selected ions, compartmentalization in cells and organs,altered cellular and organelle membrane structures, producing antioxidant com-pounds and enzymes, and using alternative biosynthetic pathways. Early studiesshowed that proline, a compatible solute as mentioned earlier, is accumulated in thesaline-stressed potatoes. Potatoes were considered as moderately salt-sensitive inearly studies. However, significant variations in salt tolerance among S. tuberosumcultivars are expected, but they have not been explored systematically. Some field,greenhouse, and in vitro evaluations have been completed as summarized inDonnelly et al. [123]. As already mentioned, plants� response to salt is also relatedto the responses to other stresses, as demonstrated by microarray analysis of leafresponses to cold and salt stresses [76].

44.6.1Mechanisms of Salt Response

Major changes in potato leaves in response to salt exposure were found to be therepression of photosystems I and II and chlorophyll synthesis, according to micro-array analyses [124]. This was mirrored by protein data in which the most drasticallydownregulated proteins were involved in photosynthesis and protein synthesis [125].In addition, changes in gene expression of carbohydrate and amino acidmetabolismsuggested that salt stress caused modifications at the metabolic level.

Studies have identified cell signaling proteins frompotatoes that are induced by saltstress, including a novel leucine-rich repeat receptor-like kinase, StLRPK1 [126], andcalcium/calmodulin signaling components ScCaM1 and ScCaM5 [91]. Catechola-mines are synthesized in response to both ABA and salt stress, and are proposed tobe stress agent compounds that play an important role in the regulation of starch–sucroseconversioninplantsandmaybeimplicatedinseveralotherfunctionsincludingwoundingandpathogen responses [127]. ExpressionofStPUB17, anUND/PUB/ARMrepeat E3 ubiquitin ligase, is upregulated by many abiotic stresses including salt, andStPUB17-silenced plants were more susceptible to both salt stress and Phytophthorainfestans [128]. Nitric oxide appears to interact with salt stress signaling according tostudiesonArabidopsis.Arabidopsismutants of theAtnOA1gene involved innitricoxidesynthesis aremore sensitive to salt stress,but transgenicexpressionofStNOA1fromS.tuberosum was able to return salt sensitivity to wild-type level [129–132].

In response to salinity, cells accumulate osmoprotectants, small molecules thatbalance the osmotic difference between the cell�s surroundings and the cytosol.Proline is a small molecule that accumulates upon salt exposure and is believedto protect cells via a mechanism similar to that proposed for drought tolerance.N-succynilarginine is induced under salt stress and it is involved in argininemetabolism that leads to the production of ornithine and proline [125]. Overexpres-sion of D1-pyrroline-5-carboxylate synthetase increases proline production andconfers salt tolerance in transgenic potato plants [133]. Lycine-betaine (GB) is acommon compatible solute that accumulates in many higher plant species inresponse to salinity, drought, and low temperature [134], but potato is betainedeficient. It has been demonstrated in a variety of studies that GB exerts protective

44.6 Salt Tolerance j1137

effects and stabilizes macromolecules, enzyme activities, and membranes understressful conditions [135, 136]. Transgenic plants with enhanced salt tolerance wereengineeredwith the ability to synthesizeGB in chloroplasts via the introduction of thebacterial choline oxidase (codA) gene under the control of an oxidative stress-inducible SWPA2 promoter [137]. Ning et al. [138] also created transgenic potatoplants expressing a gene for GB synthesis that had improved tolerances to droughtand salinity. Pruvot et al. [99] identified two proteins that accumulate in response tosalt: CDSP 32 is suggested to be involved in osmoregulation in the stroma and CDSP34 is postulated to play a role in the structural mechanisms involved in the toleranceof thylakoids to dehydration stress [99].

A cDNA microarray analysis of leaves reveals that salt stress activated severalHSPs, late-embryogenesis abundant proteins, and dehydrins [124]. The accumula-tion of HSPs can act as chaperone to facilitate the correct folding of proteins andprotect them from denaturing under stress conditions. The leaves of potatoesexposed to salt stress induced the gene expression of several HSPs [124] and salt-tolerant cultivars have a propensity to accumulate moreHSPs under salt stress [125].Cpn60b is another example of a molecular chaperone from Solanum that is inducedby salt stress [100]. These authorsfirst identified this gene alongwith several others ina functional screen for salt tolerance using a heterologous expression method in E.coli. Another of these candidate salt stress-related genes was dhn2, a dehydrin thatshares homology with the D11 group of LEA dehydrins and is synthesized duringseed desiccation and in response to salt stress.

Several hormones have been implicated in responses to salt stress. For example,calreticulin is a Ca2þ storage protein that appears to be involved in ABA-induced salttolerance. Its gene expression and protein levels are induced by salt stress [139].Furthermore, grafting experiments demonstrate that both salt stress tolerance andcalreticulin expression are regulated by the roots [139]. Experimentswith acetylsalicylicacid suggest that pretreatment induces preadaptive responses to salt andwater stressesleading to the protection of the photosynthetic pigments and the maintenance ofmembrane integrity, which is ultimately reflected in improved plant growth [140].

Salt transporters/vacuolar Naþ /Hþ antiporters have been studied for salt response.Plant cells adapting to salt stress improve cellular ion homeostasis by accumulatingorganic solutes in the cytosol, by compartmentalizing ions in the vacuole, and byexcluding extra Naþ ions from the cells. To this end, transgenic potato plantsconstitutively overexpressing an Arabidopsis tonoplast Naþ /Hþ antiporter (AtNHX1gene) were constructed but not analyzed for salt tolerance [141]. Another group byBayat et al. [142] transformed two cultivars of potatoes (S. tuberosum) with a barleyantiporter gene (HvNHX2) driven by the CaMV 35S promoter. Transgene expressionconferred a higher NaCl tolerance to one of the cultivars.

44.6.2Genes Related to Salt Tolerance

Altering potato metabolism through transgenic approaches has also altered salttolerance. Besides the genes indicated above, several others have been studied.


Transgenic plants with reduced StubGAL83 expression had increased sensitivity to saltstress, as well as impaired root and tuber development [143]. This potato gene wassuspected to be an important regulator of salt stress because it encodes a subunit of aprotein kinase complex that is similar to the yeast SNF1 and mammalian AMPKcomplexes that are modulated by changes in the cellular AMP/ATP ratio and areimportant regulators ofmetabolic and stress responses. Conversely, continuous expres-sionofaglyceraldehyde-3-phosphatedehydrogenase in transgenicpotatoplants resultedin improved tolerance against salt loading [144]. The importance of nitrogen status inmetabolism has been highlighted in salt-stressed potato plants that had increasedglutamine synthetase activity in the roots and decreased activity in the leaves [145].

Salt stress response is also related to biotic stress factors. Microarray analysis ofleaves reveals that salt stress induced the expression of several pathogenesis-relatedproteins, as well as several transcription factors related to plant defense pathways,demonstrating a crosstalk between abiotic and biotic stress responses during saltexposure [124]. In another study, 6 of 20 proteins upregulated by salt stress wereknown to play a role in plant defense (i.e., osmotin-like protein, HSPs, calreticulin,and protease inhibitors) highlighting the close link between these processes [125].For example, osmotin is a member of the pathogenesis-related family of proteins 5(PR-5), which is induced by biotic stresses and implicated in defense againstfungi [146, 147]. However, osmotin protein levels in salt-tolerant cultivars are alsoupregulated in response to salt. Furthermore, overexpression of osmotin has beenproposed to confer salt tolerance to transgenic potato plants [148]. PR-10a is anotherpathogenesis-related proteinwith increased protein expression in potato cell culturesunder salt stress. Potato cell cultures that overexpressed a PR-10a transgene wereconferred increased salt and osmotic tolerance [149].

Transcription factors are involved in osmotic stress response via ABA-dependentor ABA-independent pathways. Functional studies of several transcription factorshave demonstrated their effectiveness in mitigating salt stress [124]. For example,ArabidopsisDREB/CBF (dehydration-responsive element binding/C-repeat bindingfactor) proteins are key transactivational factors involved in environmental stressessuch as cold, drought, and salinity [105]. Improved tolerance to salinity was conferredto potato plants transformed with Arabidopsis DREB1A under the control of anArabidopsis stress-inducible promoter (rd29A) [150]. Ectopic expression of potatoStZFP1 (a TFIIIA-type zinc finger protein), also driven by rd29A, in transgenictobacco increased plant tolerance to salt stress [53]. StEREBP1 (ethylene-responsiveelement binding protein 1) is a transcription factor that binds GCC and DRE/CRTcis-elements and that responds to several environmental stresses including lowtemperature. Overexpression of StEREBP1 in potatoes enhanced their tolerance tocold and salt stress [104].

44.6.3Omics Studies

Salinity tolerance is a multigenic trait with complex regulatory factors. Significantprogress in its understanding has been made in Arabidopsis and tomato; however,


breeding for salinity tolerance in potato is still in its infancy. Several tolerant lines ofcultivated andwild species have been identified on the basis of the Center for GeneticResources (CGN)Genebank evaluation data, but breeding a tolerant line with growthvigor and yield is still a long process. To aid in this endeavor, several transcriptome-wide analyses have been performed in order to identify potato genes involved insalinity. As previouslymentioned, Rensink et al. [75, 76] profiled genes in response tosalt and temperature stresses. Other omics studies include a microarray study byLegay et al. [124] and a proteomics study by Aghaei et al. [125]. Both described theexpression of several individual genes or proteins and several functional categories ofgenes that are differentially regulated under salinity.

Salt tolerance of potato cultivars and clones in general has increased activity ofantioxidant enzymes, including SOD and peroxidase (POD) [151–153] as well asAPX, CAT, and glutathione reductase (GR) [154]. Similarly, treatments that boost theantioxidant capacity of a plant, such as exogenous application of ascorbic acid, havealso been found to ameliorate the salinity tolerance and increase the CAT and SODactivities in S. tuberosum [155].

Several examples of successful transgenic approaches have manipulated theantioxidant system to improve salt tolerance. For example, transgenic in vitro plantsexpressing a bacterial CATgene had an improvedmultiplication rate under salt stresscompared to control, while knockdown of the CAT gene reduced the multiplicationrate, tuber yield, and leaf chlorophyll content [156]. Another study expressedArabidopsis nucleoside diphosphate kinase 2, a known regulator of antioxidant geneexpression, under the control of anoxidative stress-inducible promoter (SWPA2). Thetransgenic potato plants had higher APX activity and were more tolerant to high saltconcentrations, presumably because of improved scavenging of ROS derived fromsalt stress [56]. This same research group demonstrated that transgenic potato plantsexpressing Cu/Zn SOD and APX genes in chloroplasts under the control of theSWPA2 promoter had increased tolerance to salt stress. Furthermore, retransfor-mation of these same transgenic plants with a bacterial choline oxidase (coda) gene tosynthesize glycine-betaine in chloroplast synergistically enhanced salt tolerance.Ectopic production of glycine-betaine in the chloroplast helped to maintain higheractivities of SOD,APX, andCATduring salt stress [58]. A similar transgenic approachengineered potato plants with enhanced ascorbic acid accumulation and tolerance tosalt stress by overexpression of a rat GLOase gene that is responsible for ascorbic acidproduction [157]. The T1 transgenic plants exposed to salt stress (100mM NaCl)survived better with increased shoot and root length compared to untransformedplants. The elevated level of AsA accumulation in transgenics was directly correlatedwith their ability to withstand abiotic stresses.

44.6.4Wounding

Tuber skin is a suberized layer of native periderm. It is often called skin-set. Tuberskin is used to protect tubers from pathogen infection, desiccation, and water loss.Tuber skins can be easily wounded by mishandling during harvest and postharvest


storage, resulting in decreased tuber quality and increased defects. The cultivars thatlack an effective suberization function will be more prone to tuber defects such asbruising, crack, and skinning. In some cases, within 1 h of wounding, tuber skintissues respond with wound-induced suberization [158]. The overall wound-healingprocess in potato tubers is characterized by the rapid accumulation ofwaxes to restrictwater vapor loss [159] and the development of a suberized closing layer and associatedwound periderm that resists desiccation and microbial invasion [160]. Suberizationrequires the biosynthesis of phenolic, aliphatic, and glycerol monomers and assem-bly of these monomers into polymer domains, named as suberin poly (phenolic)domain (SPPD) and suberin poly (aliphatic) domain (SPAD) [161]. Phenylalanineammonia lyase (PAL) is a major player in the regulation of wound-healing activitybecause it is required for the formation of polyphenols in the SPPD [160]. In relationto this, a proteomic analysis of the wound-healing process reveals the accumulationof several peroxidases [162] that have been postulated to participate in the cross-linking of the hydroxycinamic alcohols that constitute lignin and SPPD [163].

Three hormones have been traditionally associated with wound healing becausetheir levels dramatically increased upon wounding [164]. Most recent evidenceimplicates ABA in wound healing [164], but does not support a role for ethylenein this process, while the role of jasmonic acid remains speculative [164]. This isfurther supported by the observation that wound-healing ability declines with tuberage/storage, partly because of a reduced ability to accumulate ABA that appears tomodulate PAL activity and accumulation of suberin polyphenols [160].

Chaves et al. [162] provide insight into the proteomics behind the wound-healingprocess in tuber slices. The cell differentiation processes that were triggered by slicinglead to changes in metabolism, activation of defense, and cell wall reinforcement.Proteins detected related to storage, for example, patatin, cell growth and division,cell structure, signal transduction, energy production, disease/defense mechanisms,secondary metabolism, and suberization. Even 8 days after wounding, the proteinpatterns of slices ofwoundperidermandnative peridermwere still quite different [162].

To further understand the metabolites associated with suberization process, a GC/MS-based metabolite profiling study was conducted, using wound-healing potato(S. tuberosumL.) tubers [165].Usingprincipal component analysismethods, the authorsrevealed a separation of metabolite profiles according to different suberization stages,with clear temporal differences in the nonpolar and polar profiles. These temporaldifferences were in keeping with earlier histochemical analyses of suberin macromo-lecular assembly: first, the phenolic compounds that accumulate in response to awounding event are polymerized into the SPPD within the primary cell wall; then, thisevent is closely followed by the biosynthesis of SPAD components and their assemblyinto a multilammelar structure between the cell wall and the plasma membrane[161, 166]. Yang et al. [165] observed that the nonpolar metabolite profiles containedcharacteristic SPAD components, which appeared later than the bulk of the SPPDcomponents apparent in the polarmetabolite profiles. In the nonpolar profiles, suberin-associated aliphatics contributed themost to cluster formation, while a broader range ofmetabolites (including organic acids, sugars, amino acids, and phenylpropanoids)influenced cluster formation among polar profiles. The authors exploited strong


correlations between known suberin-associated compounds and several unidentifiedmetabolites in the profiles to identify novel compounds involved in suberin biosyn-thesis. In addition, the results distinguished between suberin-related metabolites andmetabolites associated with other wound-induced processes. For example, chlorogenicacid was clearly identified as one of the phenoic compounds induced by wounding.

In addition to suberization, wounding of potato tubers induces changes in someothermetabolites, including those that function as defense compounds, for example,hydroxycinnamoyl putrescines [165, 167] and chlorogenic acid [165, 168]. Plantsappear to have distinct signal transduction pathways that can distinguish betweeninsect damage and abiotic damage based on the presence of insect-derived elicitorsthat function to induce plant defense against herbivory [169, 170]. For example, Turraet al. [171] have demonstrated differential expression patterns of potato proteaseinhibitors in response to wounding and nematode infection. Nevertheless, duringthe wound-healing process, a number of upregulated proteins result in the produc-tion of antimicrobial compounds such as phenols and pathogenesis-related (PR)peptides or the protein themselves are PR, such as beta-1,3-glucanase (PR-2),chitinases (PR-3), osmotins (PR-5), protease inhibitors (PR-6), plant peroxidases(PR-9), and PR-10 proteins [162]. The induction of multiple protease inhibitors uponwounding [162] is of particular interest because after patatin, low molecular weightproteinase inhibitors are themost abundant group of tuber storage proteins [172] andthey have been implicated in the regulation of endogenous protease activity, proteinstabilization, modulation of apoptosis, and protection from biotic stress [173, 174].

In addition to its function in defense [165, 168], chlorogenic acid is a majorchemical involved in a nonenzymatic discoloration in potato tubers, called after-cooking darkening (ACD) [175]. This leads to another study that recently completed.Murphy et al. [176] used a comparative proteomics approach to identify proteinsrelated to potato tuber ACD, a defect not welcomed by French fry industry. Clusteringanalysis of relative quantitative proteomics data revealed a cluster of proteins whoserelative expression appeared the most positively correlated with darkening and anadditional, smaller cluster of proteins, negatively correlatedwith darkening. Perhaps,most interestingly, they observed multiple proteins related to lipid signaling andprotease inhibitor-based wound responses that are correlated with tissue darkening.The changes in relative protein abundance showed an enhanced wound responseprogram in high ACD tissues. Among the wound-induced proteins, five weresuggested by the authors for further investigation. They are polyphenol oxidase,aspartic protease inhibitor 7 precursor, 5-lipoxygenase, linoleate:oxygen oxidoreduc-tase, and patatin T5 precursor. The authors suggest this wound response occurs inparallel to an increase in polyphenol synthesis, leading to tissue darkening [176].

44.7Conclusions and Future Perspectives

Environmental stresses, both during growing season and during postharvest storage,can affect the marketable quality of the potato crop. Stresses during the growing


season reduce photosynthetic efficiency and function, resulting in variedmetabolismchanges and inhibition of the optimal growth and development of tubers. Recentefforts in genomics, transcriptomics, proteomics, and metabolomics to understandthe physiology, biochemistry, and molecular genetics of stress responses haveprovided insight into these processes. Many promising genes have been identifiedand their roles and effectiveness in stress tolerance will be tested. Unfortunately, onelast hurdle lies in the fact that traditional transgenic approaches have not beenwelcomed by consumers and agricultural policymakers of the developed world. Thisresistance has inhibited the introduction of many stress-tolerant transgenic cultivarsinto world markets thus far. Nevertheless, recent advancement in intragenicapproaches, as outlined by Rommens et al. [177, 178], show promise in developingnew cultivars while reducing concerns about the use of selection markers and genesfrom foreign species. It is very likely that some well-defined new generationintragenic potato cultivars will be successfully tested under field conditions.

The completion of the potato genome sequencing in the near future will boost thestudy of abiotic stress significantly. Many genes and markers will be identified anddeveloped using the existing breeding lines. Because of the complexity and theheterozygosity of the cultivated potato cultivars, association mapping method willbecome a more effective tool to identify genes and markers with much less time.Finally, marker-assisted selection could be more successful if omics data could beintegrated into breeding processes for new cultivar development.

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Improving Crop Resistance to Abiotic Stress (TUTEJA:PLANT STRESS OMICS O-BK) || Potato: Improving Crop Productivity and Abiotic Stress Tolerance