Photosynthetic and respiratory changes in leaves of poplar elicited by rust infection. Photosynth Res

Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Stn. Sainte-Foy, Quebec, QC, Canada.
Photosynthesis Research (Impact Factor: 3.5). 12/2009; 104(1):41-8. DOI: 10.1007/s11120-009-9507-2
Source: PubMed
ABSTRACT
Poplars are challenged by a wide range of pathogens during their lifespan, and have an innate immunity system that activates defence responses to restrict pathogen growth. Large-scale expression studies of poplar-rust interactions have shown concerted transcriptional changes during defence responses, as in other plant pathosystems. Detailed analysis of expression profiles of metabolic pathways in these studies indicates that photosynthesis and respiration are also important components of the poplar response to rust infection. This is consistent with our current understanding of plant pathogen interactions as defence responses impose substantive demands for resources and energy that are met by reorganization of primary metabolism. This review applies the results of poplar transcriptome analyses to current research describing how plants divert energy from plant primary metabolism for resistance mechanisms.

Full-text

Available from: Sebastien Duplessis
REVIEW
Photosynthetic and respiratory changes in leaves of poplar elicited
by rust infection
Ian T. Major
Marie-Claude Nicole
Se
´
bastien Duplessis
Armand Se
´
guin
Received: 18 August 2009 / Accepted: 13 November 2009 / Published online: 9 December 2009
Ó Springer Science+Business Media B.V. 2009
Abstract Poplars are challenged by a wide range of
pathogens during their lifespan, and have an innate
immunity system that activates defence responses to
restrict pathogen growth. Large-scale expression studies of
poplar–rust interactions have shown concerted transcrip-
tional changes during defence responses, as in other plant
pathosystems. Detailed analysis of expression profiles of
metabolic pathways in these studies indicates that photo-
synthesis and respiration are also important components of
the poplar response to rust infection. This is consistent with
our current understanding of plant pathogen interactions as
defence responses impose substantive demands for
resources and energy that are met by reorganization of
primary metabolism. This review applies the results of
poplar transcriptome analyses to current research describ-
ing how plants divert energy from plant primary metabo-
lism for resistance mechanisms.
Keywords Melampsora spp. Defense response
Resource mobilization Transcriptome
Introduction
Poplars are challenged by a myriad of pests during their
lifespan, including hundreds of fungal and bacterial
pathogens reported to infect Populus species. The distri-
bution and biology of the major pathogens of Populus are
well described in several reviews (Newcombe 1996;
Newcombe et al. 2001), and the rust fungi of the
Melampsora genus are of particular importance. These rust
pathogens cause epidemics of Populus species worldwide,
especially in European and North American poplar plan-
tations. Such epidemics can lead to premature defoliation
and growth loss and can be fatal for young trees after
repeated epidemics (Pinon and Frey 2005;Ge
´
rard et al.
2006). Consequently, Melampsora spp. are the subject of
most genetic and molecular studies of poplar pathosystems.
Recent molecular studies have also examined defence
responses triggered by Marssonina brunnea, the causal
agent of leaf spot disease, which is responsible for major
epidemics of poplar plantations in China. Transcriptome
and proteome approaches have been applied to studies of
poplar–pathogen interactions and provide more detailed
analyses of incompatible and compatible interactions with
different species of Melampsora (Miranda et al. 2007;
Rinaldi et al. 2007; Azaiez et al. 2009), as well as with
poplar mosaic virus (Smith et al. 2004) and Marssonina
brunnea (Zhang et al. 2007; Yuan et al. 2008).
Plants resist pathogen infection via activation of physi-
cal and biochemical defences, such as cell wall thickening
and lignin deposition, generation of reactive oxygen spe-
cies (ROS) and accumulation of secondary metabolites like
phenolic derivatives and anti-microbial proteins such as
pathogenesis-related (PR) proteins (Dixon et al. 2002; van
Loon et al. 2006; Ferreira et al. 2007). Plant defence
responses are elicited by a sophisticated innate immunity
I. T. Major (&) M.-C. Nicole A. Se
´
guin
Natural Resources Canada, Canadian Forest Service,
Laurentian Forestry Centre, 1055 du P.E.P.S, P.O. Box 10380,
Stn. Sainte-Foy, Quebec, QC G1V-4C7, Canada
e-mail: ian.major@rncan-nrcan.gc.ca
S. Duplessis
UMR 1136 INRA/Nancy Universite
´
Interactions
Arbres/Micro-organismes, Institut National de la Recherche
Agronomique, Centre de Nancy, 54280 Champenoux, France
123
Photosynth Res (2010) 104:41–48
DOI 10.1007/s11120-009-9507-2
Page 1
system that recognizes microbe-associated molecular pat-
terns (MAMPs) such as bacterial flagellin and pathogen
avirulence or effector proteins (Chisholm et al. 2006; Jones
and Dangl 2006). Recognition of MAMPs triggers broad-
spectrum resistance mechanisms such as non-host or basal
resistance, while recognition of effector proteins by plant
R-genes leads to effector-triggered immunity resulting in
an incompatible interaction. In both cases pathogen growth
is impaired. By contrast, in a compatible interaction, the
pathogen virulence proteins subvert host plant innate
immunity and pathogen growth and development proceeds
resulting in disease. During plant innate immunity, massive
reprogramming of the plant transcriptome activates a
plethora of defence mechanisms irrespective of their
effectiveness against a specific pathogen, apparently to
ensure resistance against most pathogens (Katagiri 2004;
Bolton 2009). While this strategy is probably an evolu-
tionary necessity for effective resistance elicited by con-
served MAMPs from non-host pathogens and to simplify
signalling cascades, the activation of multiple resistance
mechanisms is energy intensive. Although plant defence
responses to pathogen infection are well studied in various
pathosystems, how plants recruit the necessary energy from
energy-producing primary metabolism pathways is much
less understood. Indeed, plant transcriptome analyses dur-
ing innate immunity also highlight altered expression of
genes associated with primary metabolism, which likely
reflects the mobilization of resources for defence
responses.
In this review, we describe how pathogen infection and
the consequent host defence responses affect photosyn-
thesis and related primary metabolic processes. We rely
heavily on transcriptome analyses of poplar–rust interac-
tions, which are rapidly developing into a model patho-
system with sequenced genomes available for both host
and pathogen (Jansson and Douglas 2007). The results of
transcriptome-based studies are described in the context of
known defence-related molecular changes and are com-
pared with other plant pathosystems where appropriate.
Since direct measurements of photosynthesis parameters
and other aspects of primary metabolism have not yet been
reported for poplar during pathogen infection, this review
should serve more as a direction for future study of the
effect of pathogen infection on photosynthesis in poplar
than as a definitive description of these effects.
Poplar defence responses: increased demand for energy
and resources
Transcriptional changes of genes associated with photo-
synthesis and primary metabolism concomitant with
changes in expression of defence-related genes suggest that
plant resources are diverted for defence during poplar–rust
interactions. To date, several inducible defence mecha-
nisms have been demonstrated during pathogen infection in
Populus spp., including the strengthening of cell walls by
lignin deposition and production of anti-microbial metab-
olites and proteins (reviewed in Duplessis et al. 2009).
Lignin deposition is one of the major defence reactions
observed during incompatible and compatible poplar–rust
interactions, although it is delayed considerably in com-
patible interactions. Phloroglucinol staining revealed a
strong accumulation of monolignols surrounding rust
infection hyphae that likely reinforces physical barriers
delineated by the vasculature to restrict further pathogen
growth (Chen et al. 2000; Rinaldi et al. 2007). Transcrip-
tome analyses show up-regulation of Populus phenyl-
propanoid pathway genes associated with monolignol
synthesis and deposition after Melampsora infection,
which corroborates the increased levels of monolignols in
infected leaves (Rinaldi et al. 2007; Azaiez et al. 2009). In
addition to accumulation of lignins, condensed tannins,
which are also derived from the phenylpropanoid pathway
and have well-documented antimicrobial properties (Scal-
bert 1991), accumulate to significantly higher levels late in
compatible poplar–rust interactions (Miranda et al. 2007).
The late accumulation of tannins corresponds to the up-
regulation of genes at 6–9 dpi that encode almost all the
enzymes of flavonoid biosynthesis necessary for condensed
tannin synthesis (Miranda et al. 2007). Defence-related
genes are also induced in poplar leaves during pathogen
infection, including several that encode PR proteins as well
as a pathogen-responsive subgroup of Kunitz proteinase
inhibitors (Duplessis et al. 2009). In particular, quantitative
RT–PCR analyses have shown that a Populus PR-1
ortholog is strongly up-regulated during several incom-
patible and compatible interactions with different
Melampsora species, as well as during infection with
Marssonina brunnea (Rinaldi et al. 2007; Cheng et al.
2008; Leve
´
e et al. 2009). Together, poplar phenylpropa-
noids and protein-based defences likely play a key role in
resistance against rust infection, although poplar defence
proteins have yet to be tested for anti-microbial effects.
Nevertheless, as large carbon-based polymers and proteins,
the synthesis of defensive phenylpropanoids and proteins is
likely very energy and carbon intensive. Interestingly, the
poplar–rust transcriptome analyses also reveal up-regula-
tion of genes encoding enzymes leading to the shikimate
pathway, which generates phenylalanine precursors for the
phenylpropanoid pathway. These include enzymes of the
pentose phosphate pathway as well as DHS (3-deoxy-7-
phosphoheptulonate synthase), which performs the first
reaction of the shikimate pathway. Increased expression of
these genes concomitant with induction of genes encoding
glycolytic enzymes suggests that carbon skeletons
42 Photosynth Res (2010) 104:41–48
123
Page 2
generated by glycolysis are at least in part used for the
production of defence-related phenylpropanoids. Thus, in
response to infection of poplar leaves with rust pathogens,
the commitment of energy and resources to the production
of defence molecules can be inferred by changes in gene
expression to primary and secondary metabolic pathways.
In other plant pathosystems, the energetic requirements of
defence responses are evident by the effect these have on
plant fitness (Smedegaard-Petersen and Tolstrup 1985;
Walters and Heil 2007), though this will be harder to
determine in a perennial species such as poplar.
Poplar transcriptomes reflect the demands of defence
during rust infection
Recent transcriptome analyses have profiled early (12 h) to
late (10 days) responses in poplar leaves after inoculation
with Melampsora rust that result in incompatible interac-
tions and compatible interactions with different degrees of
host quantitative resistance (Miranda et al. 2007; Rinaldi
et al. 2007; Azaiez et al. 2009). In addition to altered
expression of defence-related genes, these studies highlight
differential expression of several genes associated with
photosynthesis during poplar–rust interactions. Such
changes in expression of photosynthetic genes are often
highlighted in studies that profile transcriptional changes in
response to biotic stress, and likely reflect the remobiliza-
tion of resources from primary metabolic pathways to
defence-related processes. To better describe how resour-
ces are allocated for defence during rust infection, we
examined available poplar transcriptome profiles to
reconstruct pathways for energy production based on
homology to Arabidopsis pathways from AraCyc (http://
arabidopsis.org/biocyc/index.jsp) and the Kyoto Encyclo-
pedia of Genes and Genomes (KEGG; http://www.genome.
jp/kegg/). Overall, genes involved with photosynthesis,
respiration and carbohydrate metabolism are differentially
expressed in response to pathogen attack in poplar leaves
(Fig. 1). In incompatible interactions with the rust fungus,
genes associated with photosynthesis, respiration and car-
bohydrate metabolism are up-regulated as early as 2 days
post-infection (dpi) (Rinaldi et al. 2007). Transcriptome
data are not available at later timepoints for incompatible
poplar–rust interactions, but the expression profiles of
several defence-related genes are transient during incom-
patible interactions and return to a basal level after 4 dpi
(Duplessis et al., unpublished data). By contrast, in com-
patible poplar–rust interactions there are few genes whose
expression changes until after 3 dpi. At 6–9 dpi in com-
patible interactions, genes associated with photosynthesis
are down-regulated, while those involved with respiration
and carbohydrate metabolism are up-regulated (Miranda
et al. 2007; Azaiez et al. 2009). Thus, these expression
changes are delayed in the compatible interactions com-
pared with the incompatible interaction, similar to the
delay of defence activation reported in the comparative
analysis of early compatible and incompatible poplar–rust
interactions (Duplessis et al. 2009). This is consistent with
other plant pathosystems in which defence reactions elic-
ited by avirulent and virulent pathogens are qualitatively
similar and only delayed in compatible interactions (Tao
et al. 2003). Moreover, changes to photosynthesis and
respiration are also delayed in compatible compared with
incompatible interactions in other plant pathosystems
(Berger et al. 2007). Finally, the transcriptional repro-
gramming of primary metabolic pathways in poplar leaves
during rust fungus infection may reflect the energy
requirements of poplar defence responses and is an indi-
cation of the high demands of defence.
Photosynthetic genes are differentially regulated after
rust infection
The photosynthetic genes up-regulated early in incompat-
ible poplar–rust interactions encode proteins of the photo-
synthetic apparatus and the Calvin cycle, which is
responsible for fixation of CO
2
(Fig. 1; Rinaldi et al. 2007).
Changes occurring at 2 dpi are very early in the progression
of rust infection in poplar leaves, considering that the
specific infection structures from which this biotrophic
fungus derives its nutrients from the plant host (i.e. haus-
toria) do not develop until *18 h post-infection. At this
stage of infection, virulent rust fungi are detected by the
host resistance (R) genes. R gene-mediated detection of the
rust triggers a rapid defence response that resists pathogen
growth and is presumably very energy intensive. Consid-
ering that induction of genes associated with photosyn-
thesis occurs early in incompatible interactions,
photosynthesis could be increased to supply the carbon
skeletons, energy and reducing equivalents required to
support a subsequent defence response. However, in most
incompatible plant–pathogen interactions, photosynthetic
activity decreases (Berger et al. 2007), though this decrease
is not necessarily associated with repression of photosyn-
thetic genes (Bonfig et al. 2006; Swarbrick et al. 2006).
The up-regulation of photosynthetic genes in incompatible
poplar–rust interactions could reflect intrinsic differences
among pathosystems, as Melampsora rusts are obligate
biotrophs that have distinct infection structures from other
pathogens (Voegele et al. 2009). Moreover, as perennial
species, poplars may employ different strategies than
annual plants to react to pathogen attacks.
By contrast, photosynthetic genes are downregulated at
6–9 dpi in compatible interactions, including genes
encoding photosystem proteins and enzymes of the Calvin
Photosynth Res (2010) 104:41–48 43
123
Page 3
Fig. 1 Expression of genes associated with primary metabolism in
leaves of poplar infected with Melampsora rust fungi. Each row of
three coloured boxes represents the expression of one or more poplar
genes that encode an enzyme or protein complex and that are
differentially expressed after infection (number of differentially
expressed genes is shown in parentheses). Note that for most
enzymes and protein complexes, multiple genes are up- or down-
regulated. For cases where several trends are apparent, the major
trends are shown by division of the coloured box. The squares within
each row represent results from the three published transcriptome
analyses of poplar–rust interactions (left to right, Rinaldi et al. 2007,
incompatible interaction, 2 days post-infection (dpi); Miranda et al.
2007, compatible interaction, 6 dpi; Azaiez et al. 2009, compatible
interaction, partial resistance, 6 dpi). A fold change colour scale
indicates the levels of induction (red, orange and yellow)or
repression (dark and light green, blue) in infected leaves relative to
control (P \ 0.05). White is no significant change (not sig.) and grey
is no probe (no prb.) assigned to the gene. Abbreviations: TCA cycle,
tricarboxylic acid cycle; mtETC, mitochondrial electron transport
chain; PSII, photosystem II; LCHB, PSII light-harvesting complex
protein; Psb, PSII protein subunit; PQ, plastoquinone; Cyt b6/f,
cytochrome b6/f; Pc, plastocyanin; PetC, photosynthetic electron
transport C; Cyt c6, cytochrome b6/f complex protein; PSI, photo-
system I; LCBHA, PSI light-harvesting complex protein; Psa, PSI
protein subunit; FNR, ferredoxin; ATPase,H?-transporting ATP
synthase; RuBisCO, ribulose-1,5-bisphosphate carboxylase oxygen-
ase; INV, invertase; GPI, glucose-6-phosphate isomerase; PFK,
phosphofructokinase; FBPA, fructose-bisphosphate aldolase; GAP-
DH, glyceraldehyde-3-phosphate dehydrogenase; PGK, phosphoglyc-
erate kinase; GPM, phosphoglycerate mutase; PPH, phosphopyruvate
hydratase; PK, pyruvate kinase; PDC, pyruvate decarboxylase;
PEPC, phosphoenolpyruvate carboxylase; CS, citrate synthase;
ACL, ATP-citrate lyase; AH, aconitate hydratase; IDH, isocitrate
dehydrogenase; OGDH, 2-oxoglutarate dehydrogenase; SCS, succi-
nyl-CoA synthetase; SDH, succinate dehydrogenase and mtETC
complex II (CII); FH, fumarate hydratase; MDH, malate dehydroge-
nase; CI, mtETC complex I; NDUF, NADH dehydrogenase ubiqui-
none flavoprotein of mtETC CI; NDH, internal/external NAD(P)H
dehydrogenase; AOX, alternative oxidase; UQ, ubiquinone; CIII,
mtETC complex III; QCR, ubiquinol-cytochrome-c reductase of
mtETC CIII; Cyt c, cytochrome c; CIV, mtETC complex IV; COX,
cytochrome oxidase of mtETC CIV
44 Photosynth Res (2010) 104:41–48
123
Page 4
cycle (Fig. 1; Miranda et al. 2007; Azaiez et al. 2009). At
these later timepoints, rust haustoria complete the patho-
genesis cycle with the production of uredia filled with
urediospores (Laurans and Pilate 1999), and so the
repression of photosynthetic genes could represent the loss
of function of photosynthetic machinery in infected tissues.
In compatible plant–pathogen interactions, photosynthesis
decreases rapidly after infection and can be correlated with
decreased expression of photosynthetic genes (Bonfig et al.
2006; Swarbrick et al. 2006). Decreased photosynthesis in
pathogen-infected tissue is proposed as a plant strategy to
switch off photosynthesis and other assimilatory metabo-
lisms in favour of respiration and other processes to gen-
erate the resources required for defence reactions.
Furthermore, spatial resolution of photosynthesis by chlo-
rophyll fluorescence imaging has shown that decreased
photosynthesis occurs near infection sites in infected plants
and is heterogeneous across an entire leaf (Berger et al.
2007). Response heterogeneity is an important consider-
ation for poplar, as foliar necrotic lesions related to the
plant hypersensitive response are highly localized in poplar
compared with other plant pathosystems (Laurans and
Pilate 1999; Rinaldi et al. 2007). If changes in the
expression of photosynthetic genes are correspondingly
localized in poplar, these changes are likely underestimated
by the transcriptome analyses. Although these changes may
not necessarily translate into changes in photosynthetic
parameters, protein levels of RuBisCO and RuBisCO
activase, key components of the Calvin cycle, decreased
during infection of poplar leaves by the fungal pathogen
Marssonina brunnea (Yuan et al. 2008). It will be impor-
tant to quantify photosynthesis parameters of infected
poplar leaves during incompatible and compatible inter-
actions to correlate altered photosynthetic flux during the
respective defence reactions.
Rust infection in poplar affects carbohydrate
metabolism
Reduced photosynthesis combined with higher demand for
energy and carbon skeletons by defence activities results in
an energy-deficiency signal that can be perceived as a
stress cue (Baena-Gonza
´
lez and Sheen 2008) and that also
enhances sink strength in infected tissues, thereby
increasing the import of carbohydrates from source tissues
(Berger et al. 2007; Bolton 2009). A source-sink transition
may occur for poplar–rust interactions, as several enzymes
of sucrose and starch metabolism are upregulated by rust
infection. In particular, PtiCIN3, a poplar cell wall
invertase (Bocock et al. 2008) is up-regulated in incom-
patible and compatible rust interactions (Fig. 1). Invertases
hydrolyze sucrose into hexose monomers, which helps
generate a sucrose concentration gradient that drives the
symplastic translocation of sugars via the phloem to sink
tissues (Roitsch and Gonza
´
lez 2004). Moreover, invertases
are the rate-limiting enzyme of the catabolism of sucrose
and are thus a critical link in source-sink status transition
(Roitsch et al. 2003). Invertase expression can also be up-
regulated by MAMPs, demonstrating that changes in sugar
metabolism are also important for microbe-triggered
immunity in plants (Roitsch and Gonza
´
lez 2004). Inter-
estingly, recent experiments showed that repression of a
cell wall invertase in tobacco impaired and delayed
defence-related processes after infection with Phytophtho-
ra nicotianae, including expression of defence genes like
PRs, formation of ROS and development of HR, permitting
the pathogen to sporulate (Essmann et al. 2008). This
demonstrates the crucial nature of increased invertase
activity and consequent acquisition of carbohydrates for
mounting a successful defence response during plant–
pathogen interactions.
Changes in carbohydrate metabolism may also reflect a
manipulation of host cell metabolism by the pathogen as a
mechanism of pathogenesis during compatible interactions.
From this perspective, an increase in sink strength in
infected tissues would greatly enhance the potential
acquisition of nutrients that benefit the pathogen. This
phenomenon has been observed in wheat epidermis cells
infected by Blumeria graminis (Sutton et al. 2007) and in
the ArabidopsisErysiphe cichoracearum pathosystem
(Fotopoulos et al. 2003). Interestingly, the rust fungus
Uromyces fabae expresses a functional hexose transporter
exclusively in the haustorium (Voegele et al. 2001), sug-
gesting that the rust haustorium serves as a sink that
competes with natural plant sinks for nutrients. However,
the increased expression of invertase was higher in resis-
tant poplar–rust interactions, strongly suggesting that this
change is related to the host defence response rather than
pathogenesis. Increased cell wall invertase activity in
poplar leaves has been shown to modulate sink strength
during herbivore defence responses and is correlated with
translocation of carbohydrates for production of defence
metabolites like condensed tannins (Arnold and Schultz
2002), which is consistent with a role for invertases in
poplar defence responses.
Rust infection in poplar affects respiration
Compared with other organisms, plant respiration has
evolved alternative enzymes that bypass respiration via an
interconnected metabolic network including photosyn-
thetic, mitochondrial and cytosolic activities (Plaxton and
Podesta 2006). This plasticity is an essential trait for sessile
organisms to survive the biotic and abiotic stresses of a
changing environment. In addition to a pivotal role in plant
growth and development, plant respiration (glycolysis, the
Photosynth Res (2010) 104:41–48 45
123
Page 5
mitochondrial tricarboxylic acid (TCA) cycle and mito-
chondrial electron transport chain (mtETC)) is stimulated
during plant defence responses elicited by pathogen chal-
lenge and provides the energy and carbon skeletons
required by resistance mechanisms (Bolton 2009). For
example, in barley inoculated with an avirulent strain of
powdery mildew (Erysiphe graminis), respiration rates
increase rapidly and are associated with a later decrease in
grain yield, indicative of a link with the energy require-
ments of defence in this incompatible interaction
(Smedegaard-Petersen and Stølen 1981). Transcriptome
analyses of poplar–rust interactions are in agreement with
such observations, as genes involved with plant respiration
are up-regulated during both incompatible and compatible
poplar–rust interactions, including genes encoding
enzymes of glycolysis, the TCA cycle and mtETC (Fig. 1).
Increased expression of genes encoding enzymes of
glycolysis and the TCA cycle during plant defence reac-
tions correlates well with changes in respiration rates. For
example, expression of phosphofructokinase, the key
enzyme of glycolysis, is up-regulated in wheat during the
Lr34-mediated response to the rust fungus Puccinia triti-
cina (Bolton et al. 2008). In potato, infection by a virulent
Phytophtora infestans strain increases gene expression of
glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and
a corresponding increase of GAPDH activity (Laxalt et al.
1996). Furthermore, Laxalt et al. (1996) suggested that
GAPDH is part of a distinct defence response that is acti-
vated late and redirects primary metabolism to produce the
metabolites required by the new physiological state. Genes
encoding both cytosolic subunits of GAPDH are up-regu-
lated during both incompatible and compatible poplar–rust
interactions. Most enzymes of the TCA cycle were up-
regulated in at least one of the three poplar–rust tran-
scriptome studies, suggesting that high flux of the TCA
cycle occurs concomitantly with defence responses.
Moreover, several genes encoding components of the
enzymatic complexes of mtETC are induced during rust
infection, which also suggests that metabolism is enhanced
in rust-challenged tissue. Interestingly, genes encoding
components of the alternative respiratory chain are also up-
regulated during incompatible and compatible poplar–rust
interactions (Fig. 1; shown as blue pathways in mtETC),
particularly the NADH dehydrogenase NDB2 and the
alternative oxidases AOX1a and AOX1d which may form a
complete alternative respiratory pathway. Alternative
respiratory pathways are associated with a high metabolic
rate and play a central role during plant stress responses
(Clifton et al. 2006; Van Aken et al. 2009). As a bypass for
oxidative respiration, alternative respiration does not pro-
duce ATP; however, it likely allows increased glycolytic
and TCA cycle flux when oxidative respiration is saturated
and is therefore crucial for the production of carbon
skeletons in times of high demand (Clifton et al. 2006).
Alternative respiration is also associated with senescence
and programmed cell death (PCD); during active defence
response, alternative respiration minimizes ROS produc-
tion during programmed cell death (Vanlerberghe et al.
2009). In Arabidopsis, AOX provides signalling homeo-
stasis in the mitochondrion by modulating the strength of
stress signalling pathways. Thus, the increased expression
of poplar AOX is a potential marker for increased metab-
olism associated with high demands of defence responses
and may also be involved in signalling following rust
infection.
Conclusion
Analyses of plant transcriptomes during plant defence
responses reveal concomitant changes in the expression of
defence and metabolic pathways, which are necessary to
support the resource demands of resistance (Bolton 2009).
These transcriptional findings have fuelled functional
studies to directly measure changes in resource allocation
during defence responses. Plant infection with rust bio-
trophs has likewise been shown to affect photosynthesis
and carbohydrate metabolism (Voegele et al. 2009). In
poplar, the redistribution of carbohydrates is crucial for
proper induction of phenylpropanoid defences in response
to insect challenge (Arnold and Schultz 2002). Recent
transcriptome and proteome analyses of poplar–pathogen
interactions also indicate the importance of regulation of
primary metabolic pathways, including photosynthesis and
carbohydrate metabolism, that occur during plant defence
responses. Because the transcriptomic studies examined
distinct Populus-Melampsora pathosystems involving dif-
ferent species of both host and parasite, the apparent
reprogramming of photosynthesis and respiration is most
likely a genuine response in poplar leaves during rust
infection. However, changes to photosynthesis and carbon
metabolism have yet to be experimentally demonstrated for
poplar–pathogen interactions. Thus, the determination of
changes in photosynthesis parameters and of other meta-
bolic pathways in response to pathogen infection will be
essential to assessing the importance of resource and
energy allocation for proper activation of resistance
mechanisms. This will be especially crucial in the context
of assessing the costs of poplar defence responses to better
understand the impact of losses to biomass accumulation
due to pathogen infections for Populus-based bioenergy
projects (Rubin 2008).
Acknowledgements The authors thank Pamela Cheers for editing
work and an anonymous reviewer for valuable comments. IM is the
recipient of a postdoctoral Visiting Fellowship in Canadian
46 Photosynth Res (2010) 104:41–48
123
Page 6
Government Laboratories from the Natural Sciences and Engineering
Research Council of Canada (NSERC). This work was supported by
grants from NSERC and the Canadian Genomics R&D Initiative to
AS and by INRA and Re
´
gion Lorraine grants to Se
´
bastien Duplessis.
References
Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite
for induced tannin biosynthesis in developing leaves of Populus.
Oecologia 130:585–593
Azaiez A, Boyle B, Leve
´
eV,Se
´
guin A (2009) Transcriptome
profiling in hybrid poplar following interactions with Melamp-
sora rust fungi. Mol Plant Microbe Interact 22:190–200
Baena-Gonza
´
lez E, Sheen J (2008) Convergent energy and stress
signaling. Trends Plant Sci 13:474–482
Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets
phytopathology: Plant primary metabolism and plant-pathogen
interactions. J Exp Bot 58:4019–4026
Bocock PN, Morse AM, Dervinis C, Davis JM (2008) Evolution and
diversity of invertase genes in Populus trichocarpa. Planta
227:565–576
Bolton MD (2009) Primary metabolism and plant defense—fuel for
the fire. Mol Plant Microbe Interact 22:487–497
Bolton MD, Kolmer JA, Xu WW, Garvin DF (2008) Lr34-mediated
leaf rust resistance in wheat: transcript profiling reveals a high
energetic demand supported by transient recruitment of multiple
metabolic pathways. Mol Plant Microbe Interact 21:1515–1527
Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006)
Infection with virulent and avirulent P. syringae strains differ-
entially affects photosynthesis and sink metabolism in Arabid-
opsis leaves. Planta 225:1–12
Chen C, Meyermans H, Burggraeve B, De Rycke RM, Inoue K, De
Vleesschauwer V, Steenackers M, Van Montagu MC, Engler GJ,
Boerjan WA (2000) Cell-specific and conditional expression of
caffeoyl-coenzyme A-3-O-methyltransferase in poplar. Plant
Physiol 123:853–867
Cheng Q, Cao YZ, Pan HX, Wang MX, Huang MR (2008) Isolation
and characterization of two genes encoding polygalacturonase-
inhibiting protein from Populus deltoides. J Genet Genomics
35:631–638
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe
interactions: shaping the evolution of the plant immune response.
Cell 124:803–814
Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in
Arabidopsis: a comparative analysis of differential expression in
the gene family provides new insights into function of non-
phosphorylating bypasses. Biochim Biophys Acta 1757:730–741
Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L (2002)
The phenylpropanoid pathway and plant defence—a genomics
perspective. Mol Plant Pathol 3:371–390
Duplessis S, Major I, Martin F, Se
´
guin A (2009) Poplar and pathogen
interactions: insights from Populus genome-wide analyses of
resistance and defense gene families and gene expression
profiling. Crit Rev Plant Sci 28:309–334
Essmann J, Schmitz-Thom I, Scho
¨
n H, Sonnewald S, Weis E, Scharte
J (2008) RNA interference-mediated repression of cell wall
invertase impairs defense in source leaves of tobacco. Plant
Physiol 147:1288–1299
Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM,
Duarte J, Borges A, Teixeira AR (2007) The role of plant
defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–
700
Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ,
Sauer N, Hall JL, Williams LE (2003) The monosaccharide
transporter gene, AtSTP4, and the cell-wall invertase, Atbfruct1,
are induced in Arabidopsis during infection with the fungal
biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829
Ge
´
rard PR, Husson C, Pinon J, Frey P (2006) Comparison of genetic
and virulence diversity of Melampsora larici-populina popula-
tions on wild and cultivated poplar and influence of the alternate
host. Phytopathology 96:1027–1036
Jansson S, Douglas CJ (2007) Populus: a model system for plant
biology. Annu Rev Plant Biol 58:435–458
Jones JDG, Dangl JL (2006) The plant immune system. Nature
444:323–329
Katagiri F (2004) A global view of defense gene expression
regulation—a highly interconnected signaling network. Curr
Opin Plant Biol 7:506–511
Laurans F, Pilate G (1999) Histological aspects of a hypersensitive
response in poplar to Melampsora larici-populina. Phytopathol-
ogy 89:233–238
Laxalt AM, Cassial RO, Sanllorenti PM, Madrid EA, Andreu AB,
Daleo GR, Conde RD, Lamattina L (1996) Accumulation of
cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA
under biological stress conditions and elicitor treatments in
potato. Plant Mol Biol 30:961–972
Leve
´
e V, Major I, Levasseur C, Tremblay L, MacKay J, Se
´
guin A
(2009) Expression profiling and functional analysis of Populus
WRKY23 reveals a regulatory role in defense. New Phytol
184:48–70
Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J,
Constabel CP (2007) The transcriptional response of hybrid
poplar (Populus trichocarpa 9 P. deltoides) to infection by
Melampsora medusae leaf rust involves induction of flavonoid
pathway genes leading to the accumulation of proanthocyani-
dins. Mol Plant Microbe Interact 20:816–831
Newcombe G (1996) The specificity of fungal pathogens of Populus.
In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM
(eds) Biology of Populus and its implications for management
and conservation. NRC Research Press, Ottawa, pp 223–246
Newcombe G, Ostry M, Hubbes M, Pe
´
rinet P, Mottet M-J (2001)
Poplar diseases. In: Dickmann DI, Isebrands JG, Eckenwalder
JE, Richardson J (eds) Poplar culture in North America. NRC
Research Press, Ottawa, pp 249–276
Pinon J, Frey P (2005) Interactions between poplar clones and
Melampsora populations and their implications for breeding for
durable resistance. In: Pei MH, McCracken AR (eds) Rust
diseases of willow and poplar. CABI Publishing, Cambridge, pp
139–154
Plaxton WC, Podesta FE (2006) The functional organization and
control of plant respiration. Crit Rev Plant Sci 25:159–198
Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A,
Wincker P, Le Thiec D, Fluch S, Martin F, Duplessis S (2007)
Transcript profiling of poplar leaves upon infection with
compatible and incompatible strains of the foliar rust Melamp-
sora larici-populina. Plant Physiol 144:347–366
Roitsch T, Gonza
´
lez M-C (2004) Function and regulation of plant
invertases: sweet sensations. Trends Plant Sci 9:606–613
Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003)
Extracellular invertase: key metabolic enzyme and PR protein. J
Exp Bot 54:513–524
Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454:841–
845
Scalbert A (1991) Antimicrobial properties of tannins. Phytochem-
istry 30:3875–3883
Smedegaard-Petersen V, Stølen O (1981) Effect of energy-requiring
defense reactions on yield and grain quality in a powdery
mildew-resistant barley cultivar. Phytopathology 71:396–399
Smedegaard-Petersen V, Tolstrup K (1985) The limiting effect of
disease resistance on yield. Annu Rev Phytopathol 23:475–490
Photosynth Res (2010) 104:41–48 47
123
Page 7
Smith CM, Rodriguez-Buey M, Karlsson J, Campbell MM (2004)
The response of the poplar transcriptome to wounding and
subsequent infection by a viral pathogen. New Phytol 164:123–
136
Sutton PN, Gilbert MJ, Williams LE, Hall JL (2007) Powdery mildew
infection of wheat leaves changes host solute transport and
invertase activity. Physiol Plant 129:787–795
Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic
consequences of susceptibility and resistance (race-specific and
broad-spectrum) in barley leaves challenged with powdery
mildew. Plant Cell Environ 29:1061–1076
Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S, Han B, Zhu T, Zou
G, Katagiri F (2003) Quantitative nature of Arabidopsis
responses during compatible and incompatible interactions with
the bacterial pathogen Pseudomonas syringae. Plant Cell
15:317–330
Van Aken O, Giraud E, Clifton R, Whelan J (2009) Alternative
oxidase: a target and regulator of stress responses. Physiol Plant
137:354–361
van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible
defense-related proteins in infected plants. Annu Rev Phytopa-
thol 44:135–162
Vanlerberghe GC, Cvetkovska M, Wang J (2009) Is the maintenance
of homeostatic mitochondrial signaling during stress a physio-
logical role for alternative oxidase? Physiol Plant 137:392–406
Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of
haustoria in sugar supply during infection of broad bean by the
rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98:8133–
8138
Voegele RT, Hahn M, Mendgen K (2009) The Uredinales: cytology,
biochemistry, and molecular biology. In: Deising HB (ed) and
Esser K (Ser ed) Plant relationships, 2nd edn. The Mycota, vol 5.
Springer, Berlin, pp 69–98
Walters D, Heil M (2007) Costs and trade-offs associated with
induced resistance. Physiol Mol Plant Pathol 71:3–17
Yuan K, Zhang B, Zhang YM, Cheng Q, Wang MX, Huang MR
(2008) Identification of differentially expressed proteins in
poplar leaves induced by Marssonina brunnea f. sp. multi-
germtubi. J Genet Genomics 35:49–60
Zhang Y, Zhang X, Chen Y, Wang Q, Wang M, Huang M (2007)
Function and chromosomal localization of differentially
expressed genes induced by Marssonina brunnea f. sp. multi-
germtubi in Populus deltoides. J Genet Genomics 34:641–648
48 Photosynth Res (2010) 104:41–48
123
Page 8
  • Source
    • "Further work is required to determine whether these substantial physical changes are directly analogous with a hypersensitive response and triggered by R-gene protein signalling. The putative reprogramming of primary carbon metabolism between photosynthesis (down-regulation of transcripts associated with photosystem II–BIN 1.1) and cell wall strengthening (BIN 10) observed in this study has been noted frequently in response to fungal, bacterial and virus attack525354, and less commonly following insect attack [55]. The concept of resistance induction coming at a physiological cost to plant, is widely accepted, regardless of the type of biotic or abiotic elicitor [56]. "
    [Show abstract] [Hide abstract] ABSTRACT: The kiwifruit cultivar Actinidia chinensis 'Hort16A' is resistant to the polyphagous armoured scale insect pest Hemiberlesia lataniae (Hemiptera: Diaspididae). A cDNA microarray consisting of 17,512 unigenes selected from over 132,000 expressed sequence tags (ESTs) was used to measure the transcriptomic profile of the A. chinensis 'Hort16A' canes in response to a controlled infestation of H. lataniae. After 2 days, 272 transcripts were differentially expressed. After 7 days, 5,284 (30%) transcripts were differentially expressed. The transcripts were grouped into 22 major functional categories using MapMan software. After 7 days, transcripts associated with photosynthesis (photosystem II) were significantly down-regulated, while those associated with secondary metabolism were significantly up-regulated. A total of 643 transcripts associated with response to stress were differentially expressed. This included biotic stress-related transcripts orthologous with pathogenesis related proteins, the phenylpropanoid pathway, NBS-LRR (R) genes, and receptor-like kinase-leucine rich repeat signalling proteins. While transcriptional studies are not conclusive in their own right, results were suggestive of a defence response involving both ETI and PTI, with predominance of the SA signalling pathway. Exogenous application of an SA-mimic decreased H. lataniae growth on A. chinensis 'Hort16A' plants in two laboratory experiments.
    Full-text · Article · Nov 2015 · PLoS ONE
    • "During susceptible responses, poplar genes associated with photosynthesis were downregulated while genes associated with carbon metabolism and respiration were upregulated 6 to 9 d after initial attack (Miranda et al. 2007, Azaiez et al. 2009). In susceptible plants, downregulation of photosynthesis has been proposed as a plant strategy to favor processes like respiration over assimilatory metabolic processes to generate defense resources (Major et al. 2010), whereas in resistant plants, the upregulation of various genes associated with photosynthesis has been proposed to supply the carbon skeletons, energy, and reducing equivalents needed to mount defenses against invaders. As the leaf tissue sampled for these investigations with poplar trees was located near (on the same leaf) infection sites, these results would be most comparable with our results for leaf three (the directly attacked leaf), which showed a slight increases of photosynthesis for both resistant and susceptible Hessian fly-attacked plants. "
    [Show abstract] [Hide abstract] ABSTRACT: Gall-inducing insects are known for altering source-sink relationships within plants. Changes in photosynthesis may contribute to this phenomenon. We investigated photosynthetic responses in wheat [Triticum aestivum L. (Poaceae: Triticeae)] seedlings attacked by the Hessian fly [Mayetiola destructor (Say) (Diptera: Cecidomyiidae], which uses a salivary effector-based strategy to induce a gall nutritive tissue in susceptible plants. Resistant plants have surveillance systems mediated by products of Resistance (R) genes. Detection of a specific salivary effector triggers downstream responses that result in a resistance that kills neonate larvae. A 2 × 2 factorial design was used to study maximum leaf photosynthetic assimilation and stomatal conductance rates. The plant treatments were-resistant or susceptible wheat lines expressing or not expressing the H13 resistance gene. The insect treatments were-no attack (control) or attack by larvae killed by H13 gene-mediated resistance. Photosynthesis was measured for the second and third leaves of the seedling, the latter being the only leaf directly attacked by larvae. We predicted effector-based attack would trigger increases in photosynthetic rates in susceptible but not resistant plants. For susceptible plants, attack was associated with increases (relative to controls) in photosynthesis for the third but not the second leaf. For resistant plants, attack was associated with increases in photosynthesis for both the second and third leaves. Mechanisms underlying the increases appeared to differ. Resistant plants exhibited responses suggesting altered source-sink relationships. Susceptible plants exhibited responses suggesting a mechanism other than altered source-sink relationships, possibly changes in water relations that contributed to increased stomatal conductance.
    No preview · Article · Jun 2015 · Environmental Entomology
  • Source
    • "Among the 'darkgreen' genes, At5g64040 (probeset 247320_at) that encodes a subunit of photosystem I reaction center displayed the greatest down-regulation across all infections analyzed (median log 2 fold change: -0.86; S2 Table). Global down-regulation of photosynthetic genes is considered a common plant response to pathogen and insect attack3132333435. Inhibition of the photosynthetic activity causes a switch from primary metabolism towards non-assimilatory (e.g., carbon-consuming) pathways, which can enhance the production of anti-microbial metabolites and the expression of defense-related genes [36]. "
    [Show abstract] [Hide abstract] ABSTRACT: Intricate signal networks and transcriptional regulators translate the recognition of pathogens into defense responses. In this study, we carried out a gene co-expression analysis of all currently publicly available microarray data, which were generated in experiments that studied the interaction of the model plant Arabidopsis thaliana with microbial pathogens. This work was conducted to identify (i) modules of functionally related co-expressed genes that are differentially expressed in response to multiple biotic stresses, and (ii) hub genes that may function as core regulators of disease responses. Using Weighted Gene Co-expression Network Analysis (WGCNA) we constructed an undirected network leveraging a rich curated expression dataset comprising 272 microarrays that involved microbial infections of Arabidopsis plants with a wide array of fungal and bacterial pathogens with bio-trophic, hemibiotrophic, and necrotrophic lifestyles. WGCNA produced a network with scale-free and small-world properties composed of 205 distinct clusters of co-expressed genes. Modules of functionally related co-expressed genes that are differentially regulated in response to multiple pathogens were identified by integrating differential gene expression testing with functional enrichment analyses of gene ontology terms, known disease associated genes, transcriptional regulators, and cis-regulatory elements. The significance of functional enrichments was validated by comparisons with randomly generated networks. Network topology was then analyzed to identify intra-and inter-modular gene hubs. Based on high connectivity, and centrality in meta-modules that are clearly enriched in defense responses , we propose a list of 66 target genes for reverse genetic experiments to further dissect the Arabidopsis immune system. Our results show that statistical-based data trimming prior to network analysis allows the integration of expression datasets generated by different groups, under different experimental conditions and biological systems, into a functionally meaningful co-expression network.
    Full-text · Article · Mar 2015 · PLoS ONE
Show more