Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions

Journal of Experimental Botany, Vol. 58, No. 15/16, pp. 4019–4026, 2007

doi:10.1093/jxb/erm298

REVIEW ARTICLE

Plant physiology meets phytopathology: plant primarymetabolism and plant–pathogen interactions

Susanne Berger1,*, Alok K. Sinha2 and Thomas Roitsch1

1 Julius-von-Sachs-Institut fuer Biowissenschaften, Universitaet Wuerzburg, Julius-von-Sachs-Platz 2,97082 Wuerzburg, Germany2 National Institute for Plant Genome Research, Aruna Asaf Ali Road, New Delhi 110067, India

Received 9 August 2007; Revised 26 October 2007; Accepted 2 November 2007

Abstract

Phytopathogen infection leads to changes in second-

ary metabolism based on the induction of defence

programmes as well as to changes in primary metab-

olism which affect growth and development of the

plant. Therefore, pathogen attack causes crop yield

losses even in interactions which do not end up with

disease or death of the plant. While the regulation of

defence responses has been intensively studied for

decades, less is known about the effects of pathogen

infection on primary metabolism. Recently, interest in

this research area has been growing, and aspects of

photosynthesis, assimilate partitioning, and source–

sink regulation in different types of plant–pathogen

interactions have been investigated. Similarly, phyto-

pathological studies take into consideration the phys-

iological status of the infected tissues to elucidate the

fine-tuned infection mechanisms. The aim of this

review is to give a summary of recent advances in the

mutual interrelation between primary metabolism and

pathogen infection, as well as to indicate current

developments in non-invasive techniques and impor-

tant strategies of combining modern molecular and

physiological techniques with phytopathology for fu-

ture investigations.

Key words: Carbohydrate metabolism, pathogen infection,

photosynthesis.

Plant–pathogen interactions

Plant pathogens include fungi, bacteria, oomycetes, andviruses. Pathogens have devised different strategies toinvade a plant, as well as to feed on and reproduce in the

plant. Besides the assignment to bacteria or fungi, this isregarded as an important feature to classify the attackingmicro-organism (Oliver and Ipcho, 2004). Biotrophicpathogens need living tissue for growth and reproduction;in many interactions the tissue will die in the late stages ofthe infection (hemi-biotrophic pathogens). By contrast,necrotrophic pathogens kill the host tissue at the begin-ning of the infection and feed on the dead tissue. Viruses,in general, need living tissue for nutrition, while bio-trophic as well as necrotrophic strategies can be foundamong bacteria and fungi. Similarities in the pathwaysinvolved in the defence of the plants against biotrophicfungi and bacteria on one hand or against necrotrophicfungi and bacteria on the other hand have been described.The jasmonate/ethylene pathway is more important indefending necrotrophic pathogens while salicylic acid-dependent responses are more effective against biotrophicpathogens (Thomma et al., 2001).Pathogens can also be divided according to the environ-

ment in which they occur and the tissues which they infect.A common classification is to distinguish between above-and below-ground tissues as the primary target of thepathogen. Related to this, above-ground tissue might begreen, assimilate-producing tissue, typically source leaves,or assimilate-importing tissue such as flowers. Pathogensinfecting source tissue will encounter different conditionsrelated to primary metabolism as well as to defenceresponses compared with those pathogens infecting sinkor assimilate-producing tissue such as roots, flowers, andsink leaves. The investigation and the understanding ofinteractions with source-(leaf)-pathogens is more advancedand, therefore, this review will focus on these interactions.Plants are resistant to the majority of micro-organisms

based on preformed and induced defence mechanisms.Recognition of the presence of micro-organisms is the first

* To whom correspondence should be addressed: E-mail: [email protected]

ª The Author [2007]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.For Permissions, please e-mail: [email protected]

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step for the activation of defence responses. Basalresistance begins with the recognition of elicitors whichare derived from the micro-organisms, and similarities inthe recognition of pathogen-associated molecular patterns(PAMPs) in animals and in plants have been documented(Nuernberger and Scheel, 2001; Nuernberger and Lipka,2005). Upon contact with pathogens or with non-patho-genic micro-organisms or elicitors, ion fluxes, phosphory-lation/dephosphorylation of proteins, and the productionof signalling molecules such as salicylic acid, jasmonicacid, ethylene, and reactive oxygen species are activated.This leads to the regulation of gene expression and theinduction of defence responses, for example, cell wallstrengthening and the accumulation of phytoalexins andpathogenesis related (PR) proteins (Dangl and Jones,2001; Garcia-Brugger et al., 2006). According to thecurrent model, some micro-organisms became virulent bythe production of effector molecules which contribute totheir virulence, for example, by the suppression of plantdefence (Jones and Dangl, 2006). In these compatibleinteractions the virulent pathogen can spread in thesusceptible plant.Specific resistance is based on the recognition of the

activity of these effector molecules by plant receptorproteins. In these incompatible interactions the plant isresistant and can successfully prevent the pathogenspreading. The successful defence is based on the earlyrecognition of avirulent strains of plant pathogens and thefast activation of defence (Jones and Dangl, 2006).Furthermore, the recognition of the avirulent strainsactivates, in addition to the already mentioned defencereactions, a localized programmed cell death which canefficiently halt the spreading of biotrophic pathogens(Heath, 2000).

Effects on photosynthesis, sugar accumulation,and sink metabolism

Photosynthesis

There are obvious reasons why a contact with pathogensalters plant primary metabolism. It has been shown thatthe induction of defence is cost-intensive (Heil andBostock, 2002; Swarbrick et al., 2006). This causes anincreased demand for assimilates in the plant. In addition,the pathogen tries to manipulate plant carbohydratemetabolism for its own need, which is, for example,evident in the production of opines in plants infected withAgrobacterium tumefaciens. The withdrawal of nutrientsby the pathogen will further increase the demand forassimilates. Furthermore, pathogen infection often leads tothe development of chlorotic and necrotic areas and toa decrease in photosynthetic assimilate production. Theeffect on photosynthesis can be analysed by monitoring invivo chlorophyll fluorescence. This method is based on

measuring the fluorescence of chlorophyll a in a dark-adapted plant and after saturating light pulses (Schreiberet al., 1986; Schreiber, 2004). This fluorescence is a verysensitive marker for the efficiency of photosynthesis sincethe energy of absorbed photons can either be used forphotosynthetic electron transport or the energy will bedissipated as heat or fluorescence (van Kooten and Snel,1990). Therefore, chlorophyll fluorescence responds to thechanges in energy conversion at photosystem II reactioncentres and is also sensitive to any limitations in the darkenzymatic steps of the complex process of photosynthesis(Govindjee, 2004). Analysis of chlorophyll fluorescence isnon-invasive and therefore time-courses can be performedon the same plant material.Using this method, down-regulation of effective photo-

system II quantum yield in compatible interactions withbiotrophic as well as necrotrophic pathogens has beenreported. This comprises interactions with biotrophicbacteria such as Pseudomonas syringae (Bonfig et al.,2006), biotrophic fungi such as Albugo candida (Chouet al., 2000), Puccinia coronata and Blumeria graminis(Scholes and Rolfe, 1996; Swarbrick et al., 2006), as wellas necrotrophic fungi such as Botrytis cinerea (Bergeret al., 2004) and viruses such as tobacco mosaic virus andabutilon mosaic virus (Balachandran et al., 1994; Lohauset al., 2000; Perez-Bueno et al., 2006). In several cases,changes in chlorophyll fluorescence were detectableearlier than symptoms were visible by eye demonstratingthe sensitivity of this technique.A substantial advancement of chlorophyll fluorescence

analysis is chlorophyll fluorescence imaging (Oxborough,2004, and references therein). In addition to monitoringthe temporal dynamics, this method enables the spatialresolution of photosynthesis. Figure 1 illustrates anexample of the application of chlorophyll fluorescenceimaging to an Arabidopsis leaf infected with two differentpathogens, P. syringae on one half and B. cinerea on theother half. Using chlorophyll fluorescence imaging, it wasreported that, in general, the changes in photosynthesisupon infection are local. In addition, the imagingtechnology revealed the complexity and heterogeneity ofeffects. In Arabidopsis leaves infected with A. candidaand in tomato plants infected with B. cinerea a ring ofenhanced photosynthesis was detectable surrounding thearea with decreased photosynthesis at the infection site. Atpresent it is not clear if this stimulation of photosynthesisis due to the defence strategy of the plant.A decrease in photosynthesis has also been reported in

incompatible interactions (Scharte et al., 2005; Bonfiget al., 2006; Swarbrick et al., 2006). A direct comparisonof the interaction of Arabidopsis with a virulent and anavirulent strain of P. syringae showed that the majordifference in the changes in photosynthesis was the speedof the effects. A decrease in photosynthesis was detectableearlier with the avirulent strain than with the virulent

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strain. This indicates a similarity between the effects onprimary and secondary metabolism since, in both cases,reactions are earlier in the incompatible interaction whilequalitatively the responses in both interactions are similar(Tao et al., 2003). Chlorophyll fluorescence imaging oftobacco leaves in a macro- and microscopic scale duringan incompatible interaction with Phytophthora nicotianaerevealed that the decline in photosynthesis is a highlylocalized process which occurs in single mesophyll cells(Scharte et al., 2005). The results led to the proposal thatplants switch off photosynthesis and other assimilatorymetabolism to initiate respiration and other processesrequired for defence. Also in compatible and incompatibleinteractions between barley and B. graminis causingpowdery mildew, photosynthesis was decreased (Swarbricket al., 2006). Quantitative imaging of chlorophyll fluores-cence showed that photosynthesis was reduced both incells directly below the fungal colonies and in adjacentcells during the compatible interaction.Expression of sugar-regulated photosynthetic genes,

such as the small subunit of ribulose-1,5-bisphosphatecarboxylase (RbcS) and chlorophyll a,b binding protein(Cab) was analysed and, in most cases, in agreement withthe results of chlorophyll fluorescence analysis, a down-regulation of the expression after pathogen infection wasreported. However, in two incompatible interactions, no

repression of photosynthetic genes was detectable eventhough photosynthetic activity decreased (Bonfig et al.,2006; Swarbrick et al., 2006). This indicates that a de-crease in photosynthetic activity is not necessarily pre-ceded by the repression of photosynthetic genes.

Sink metabolism and sugar accumulation

The down-regulation of photosynthesis and the simulta-neous increased demand for assimilates very often leads toa transition of source tissue into sink tissue during plant–pathogen interactions. One indication for the induction ofa sink status in infected leaves is the increase of cell wallinvertase activity. Cell wall invertases are extracellularenzymes which cleave sucrose in the apoplast into glucoseand fructose. The resulting hexoses are transported byhexose transporters into the cell. Therefore, extracellularinvertases are important for apoplastic phloem unloadingand key enzymes in determining sink strength (Roitschet al., 2003). The cleavage of extracellular sucrose willalso result in the decreased export of assimilates from thetissue. Enhanced expression and activity of cell wallinvertases has been reported in several plant–pathogeninteractions (Benhamou et al., 1991; Chou et al., 2000;Fotopoulos et al., 2003; Berger et al., 2004; Bonfig et al.,2006; Swarbrick et al., 2006). Similarly, reduced sucrose

Fig. 1. Chlorophyll fluorescence imaging of plant–pathogen interactions. A leaf of Arabidopsis was infected with B. cinerea on the upper half of theleaf and 24 h later with a virulent strain of P. syringae on the lower half of the leaf. Measurements were performed 6 h and 48 h after the P. syringaeinfection. Shown are false colour images of the maximum PSII quantum yield (A, C) and effective PSII quantum yield (B, D). The first time pointcorresponding to 6 h after inoculation with P. syringae and 30 h after inoculation with B. cinerea is shown in (A) and (B). The second time pointcorresponding to 48 h after inoculation with P. syringae and 72 h after inoculation with B. cinerea is shown in (C) and (D).

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export from infected source leaves has been observed(Scharte et al., 2005). Even though a role for extracellularinvertases in plant–pathogen interaction has been sug-gested in all of these studies, details of the causalrelationship between this increase in invertase activityand the outcome of the interaction are still not clear (seebelow).Even though the repression of photosynthesis and the

induction of sink metabolism seem to be a generalresponse to pathogen infection, the effect on sugar levelsvaries considerably between different plant–pathogeninteractions. Infection of tobacco with tobacco mosaicvirus or P. nicotianae, of wheat with Puccinia graminisand of Arabidopsis with A. candida results in an increasein the levels of soluble sugars (Wright et al., 1995; Chouet al., 2000; Herbers et al., 2000; Scharte et al., 2005). Bycontrast, sugar levels in Arabidopsis are not altered byinfection with P. syringae and decrease in tomato plantsafter inoculation with B. cinerea (Berger et al., 2004;Bonfig et al., 2006) as well as in sunflowers treated withSclerotinia sclerotiorum (Jobic et al., 2007). In thetomato–grey mould interaction, levels of sucrose decreasemore than the levels of hexoses, leading to an increase inthe hexose-to-sucrose ratio. This increase in the hexose-to-sucrose ratio could be due to the enhanced activity ofinvertases. For many of the studies, sugar levels have beendetermined from a region containing a large area of andaround the infection site. The analysis of sugar levels andinvertase activity in infected versus uninfected regions ofan inoculated leaf showed only strong effects in theinfected region (Chou et al., 2000; Swarbrick et al.,2006). This strongly supports the importance of spatialresolution and indicates that most measurements missed orunderestimated changes. In addition, it would be desirableto distinguish between intracellular and apoplastic sugarlevels, and protocols for the isolation of apoplastic fluidhave been described (Lohaus et al., 2001). Severalpathogens live in the apoplast, therefore, extracellularassimilate levels might be more relevant for the pathogenthan intracellular levels. Scharte et al. (2005) reported anincrease in the levels of apoplastic sucrose and hexoselevels as well as invertase activity in tobacco afterinfection with P. nicotianae. The use of methods pro-viding information on the spatial distribution of com-pounds on the organ-, tissue-, and subcellular level isnecessary to elucidate the effects.Sugars are not only nutrients needed for growth,

respiration, and the accumulation of storage compounds,but, in addition, sugars are signals which can regulategene expression (Koch, 1996). For instance, the down-regulation of photosynthetic genes has been attributed tothe accumulation of hexose sugars (Scholes et al., 1994;Chou et al., 2000; Pego et al., 2000; Berger et al., 2004).Using photoautotrophic cell cultures of tomato or Cheno-podium rubrum, it was shown that treatment with fungal

elicitors or glucose resulted in a rapid decrease inphotosynthesis and later in the down-regulation ofphotosynthetic gene expression and the induction of cellwall invertase expression (Ehness et al., 1997; Sinhaet al., 2002). Similarly to the response to avirulent strainsmentioned above, a decrease in net photosynthesis is alsonot preceded by the repression of photosynthetic genes inthese systems. These data strongly suggest that thereduction in the rate of photosynthesis is a fast andimmediate effect of pathogen infection, while down-regulation of photosynthetic gene expression is a slowerprocess.Models for the regulation of carbohydrate metabolism

and photosynthesis by elicitors or pathogens have beenproposed earlier (Roitsch, 2004; Walters and McRoberts,2006). Figure 2 presents a model for the most investigatedtype of interaction, the infection with virulent biotrophicsource pathogens. Pathogen attack first initiates a series ofrapid changes resulting in a decline in photosynthesis andan increase in respiration, photorespiration, and invertaseenzyme activity. The mechanisms and pathways whichmediate these rapid changes are largely unknown.The electrophilic oxylipin 12-oxo-phytodienoic acid isa compound which has been shown to accumulate afterpathogen infection and to result in a decrease inphotosynthesis very shortly after application, suggestingthat it might be involved in the decrease in photosynthesisupon pathogen challenge (Berger et al., 2007). Hexosesreleased by the action of increased invertase activity act assignalling molecules and repress photosynthetic genes.This down-regulation of photosynthetic genes, in turn,again decreases the net photosynthesis rate (Fig. 2). Whilethe data from several plant–pathogen interactions, espe-cially with virulent biotrophic fungal pathogens, fit intothis general model, there are also some examples thatdiffer in distinct points from this model. As discussedabove, the accumulation of hexoses and the repression ofphotosynthetic genes have not always been observed.Another example is that the expression, but not theactivity, of cell wall invertases is increased in theArabidopsis–P. syringae interaction. These exceptionsfrom the rule support the complexity of the interactionswhich is based on the fundamental diversity of the plantas well as the microbial partner. As discussed above, inthis context it has to be taken into account that theanalysis of gene expression and sugar levels typicallyintegrates over a bigger area so that local effects observedby imaging techniques might not be detectable.

Relevance of the regulation of carbohydratemetabolism for plant–pathogen interactions

Even though several reports describe the effect ofpathogen infection on carbohydrate metabolism, there isstill a considerable lack of knowledge regarding how these

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changes influence the outcome of plant–pathogen inter-actions. There are several factors contributing to thecomplexity of the mutual relation between carbohydratestatus and development of disease/resistance. First, asdiscussed above, the carbohydrate status affects thedefence as well as general metabolism of the plant.Second, sugars are not only nutrients and signals for theplant partner but also for the microbial partner. Therefore,changes in assimilate levels may influence the spreadingof the pathogen and might regulate gene expression of thepathogen. Third, certain pathogens also possess extracel-lular sucrolytic enzymes such as invertases, fructoexohy-drolases, and levansucrases. The presence of extracellularinvertases has been observed in B. cinerea and Uromycesfabae (Geissmann et al., 1991; Voegele et al., 2006) andsuggested for A. candida (Chou et al., 2000). Withexpression of these enzymes the pathogen would be ableto alter the hexose and sucrose levels in the apoplast (Fig.2). It still needs to be investigated if these microbialsucrolytic activities are important for pathogenicity. Thisimplies that the investigation of the plant side needs to becomplemented by the analysis of the microbial part.Functional approaches are necessary to elucidate how

alterations in carbohydrate metabolism affect diseasedevelopment and resistance induction. In one transgenicapproach, tobacco plants constitutively expressing a yeastinvertase were generated (von Schaewen et al., 1990).Expression of the yeast-derived invertase in the cell wallof tobacco and Arabidopsis plants leads to the accumula-

tion of carbohydrates and the inhibition of photosynthesisand strongly influences growth. These plants also showedincreased defence gene expression and enhanced resistanceagainst tobacco mosaic virus (Herbers et al., 1996). This isin agreement with the induction of defence reactions byhexoses generated by increased invertase activity. Anotherfunctional approach to study the role of invertases is theanalysis of knock-out or antisense plants. Arabidopsisplants containing a single knock-out in each of the fourcell wall invertase genes did not show an obvious alterationin resistance against P. syringae or A. brassicicola (CBandulet, S Berger, T Roitsch, unpublished observation).This lack of clear effects might be due to redundancy. Onestrategy to overcome this problem is the modulation ofinvertase activity on a post-translational level. Protein-aceous inhibitors of invertases are produced by higherplants. Down-regulation of invertase activity by these plantinvertase inhibitors could be used to study the function ofinvertases. This approach has already been successfullyapplied to investigate their role in senescence (BalibreaLara et al., 2004). Other post-translational regulatorymechanisms are currently not known (Huang et al., 2007).

Summary and future perspectives

The down-regulation of photosynthesis and the inductionof sink metabolism have been regarded as generalresponses of source tissue to infection. As described

Fig. 2. Model of changes in carbohydrate metabolism in response to infection with virulent, biotrophic pathogens. Components concerning themicrobial partner are encircled.




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above, the comparison of the changes induced by differentpathogens revealed the complexity and divergence of theresponses. Therefore, careful investigations of differentaspects of carbohydrate metabolism in each pathosystemare required to understand the basis of the interaction inmore detail. While the changes caused by infection withvirulent biotrophic fungi are the best understood, researchis needed to elucidate the interaction with biotrophicbacteria, viruses, and necrotrophic pathogens as well asavirulent micro-organisms. This applies also to interac-tions in which sink organs such as roots, flowers, andstems are the first targets. Source tissue, as an assimilateexporting tissue, has a completely different carbohydratestatus and enzymatic constitution than sink tissue. Thedata obtained with source pathogens would lead to theexpectation that, due to the increased demand forassimilates, infection of sink tissue leads to a furtherincrease in sink metabolism. In agreement with thishypothesis, extracellular invertase accumulated in tomatoroots infected with Fusarium oxysporum (Benhamouet al., 1991) and expression of sucrose synthase andstarch synthase was induced in roots infected withPlasmodiophora brassicae (Siemens et al., 2006).Tumours induced by Agrobacterium tumefaciens inArabidopsis also showed increased expresssion of severalsucrose-degrading enzymes (Deeken et al., 2006). Inaddition, data obtained from symbiotic interactions alsoindicate regulation of carbohydrate fluxes; one example isthe induction of invertase and sucrose synthase inmycorrhizal arbuscules (Blee and Anderson, 2002;Schaarschmidt et al., 2006). Besides the effects oncarbohydrate metabolism, the molecular mechanisms ofregulation will be interesting to elucidate. As discussedabove, one of the important and basic mechanismsgenerally believed to contribute to up-regulation ofdefences and down-regulation of photosynthesis in theinteraction of pathogens with source tissue are theincreases in hexose levels or the increase in the hexose-to-sucrose ratio. In sink tissue, this ratio is already veryhigh but, nevertheless, infection leads to further stimula-tion of sink metabolism. In addition, despite high hexoselevels, sink tissues do not exhibit constitutively activateddefence and general resistance. This indicates that a com-bination of metabolic signals such as hexoses andphytohormone signals is responsible for regulation ofcarbohydrate and defence metabolism.There are several technical future directions which need

to be pursued in order to elucidate the connection betweenpathogen infection and plant primary metabolism. Meth-ods for spatial analysis of metabolites, for example,sucrose, glucose, and ATP at the single cell dimensionhave been reported (Mueller-Klieser and Walenta, 1993;Borisjuk et al., 2002). The application of the non-invasivemethod of chlorophyll fluorescence imaging has revealedthe importance of analysing spatio-temporal changes. The

use of different measuring protocols combined with non-biased approaches for data analysis (Matous et al., 2006)should improve the identification of pathogen-inducedfluorescence signatures. Imaging a combination of pro-cesses such as gene expression, assimilate and secondarymetabolites levels, and microbial spreading should furtherenrich stress physiological studies. Non-invasive techni-ques such as fluorescence-labelled pathogens, reportergene expression, 11C-labelled assimilates (Schwachtjeet al., 2006), FRET sugar nanosensors (Deuschle et al.,2006), multicolour fluorescence imaging (Chaerle et al.,2007; Lenk et al., 2007), and spontaneous photonemission (Bennett et al., 2005) are available.As already pointed out, functional approaches to

modulate carbohydrate metabolism and signalling arerequired to investigate how the carbohydrate status andits regulation influence plant–pathogen interactions.Most research focuses, for obvious reasons, either on

the plant side or on the pathogen side. A combination ofinvestigations of both partners including modern imagingtechnology and functional approaches is of centralimportance to understand the molecular and physiologicalbasis for plant–pathogen interactions. This knowledge willalso support the development of strategies to increasepathogen resistance in plants for practical applications.

Acknowledgements

We apologize to the colleagues whose work was not cited due tospace limitations. This work was supported by BayerischesStaatsministerium fur Umwelt, Gesundheit und Verbraucherschutzand the SFB 567.

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Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions