ReviewBacteria and fungi controlling plant growth by manipulating auxin: Balance between development and defense☆
Introduction
Plant growth and development is controlled by many signaling molecules, the so-called plant hormones, but these are also sometimes signals for defense responses. In their natural environment plants have to cope with a plethora of different organisms by which they are challenged. They have therefore developed many resistance mechanisms, using different cues for the recognition of a diverse range of pathogens. As outlined by Mausz and Pohnert (2015) metabolic properties are relevant for the defense status not only for single cells but also for whole organisms. In many cases the defense response is induced, but on behalf of the fitness of the plant. This could be a dilemma, because the balance between defense and beneficial growth responses has to be maintained. Plant hormones can integrate the response to developmental and environmental cues and thus limit defense-associated fitness costs. Many plant hormones, especially those controlling plant growth responses, fit into this category (reviewed in Denancé et al., 2013), but here auxin will be taken as an example to explain the concept of “balance between benefit and pathogen”. In plant–pathogen interactions the term “race of arms” has been coined to describe the ongoing co-evolution of defense and colonization strategies between the two partners (Anderson et al., 2010). This term could also be adjusted for the growth promotion (for instance by nitrogen fixation, see Gresshoff et al., 2015) vs. defense responses. If the hormonal balance is on the plant's side, then the plant will “win the race”, but when the pathogen can turn the hormonal system to its own advantage, the pathogen is the “winner”. The pathways to be regulated by hormones include direct defense pathways, nutritional aspects, but also cell wall maintenance (reviewed in López et al., 2008).
Auxins play many different roles in plant growth and development (Davies, 2010). On the cellular levels they are involved in the regulation of cell division, cell expansion, cell differentiation and polarity. On the whole plant levels they also contribute to organ development, such as roots (lateral and adventitious), shoots (i.e. apical dominance), leaves, as well as flower organs and fruits. They are also involved in vascular patterning and orientation in the environment (e.g. gravi- and phototropism). These examples indicate their roles in all major developmental processes of a plant. Auxins are also involved in the regulation of changes in different growth processes associated with pathogens and symbionts. While pathogens can alter the auxin response to induce specific disease symptoms during disease development, beneficial microorganisms interfere with the auxin metabolism of the host plant to induce plant growth for their own benefit (for review see Ludwig-Müller, 2014).
Even though auxin has long been recognized as a regulator of plant defense, the molecular mechanisms involved have been only recently taken under investigation. Similar to the signaling pathways of the defense-associated compounds salicylic acid (SA) and jasmonic acid (JA), auxin signaling differentially affects resistance to various pathogen groups (reviewed in Kazan and Manners, 2009). Recent evidence suggested that the auxin and SA pathways act antagonistically during plant defense reactions, whereas auxin and jasmonate pathways have many similarities regarding plant defense responses (Kazan and Manners, 2009). Auxin may also affect disease outcomes indirectly through effects on plant development (Gil et al., 2001). The evolutionary reasons behind the antagonistic interactions between SA and auxin might be that plants divert limited resources to defense-related processes at the expense of plant growth when attacked by a pathogen (Kazan and Manners, 2009). The growth of plants is dependent on energy, mainly from photosynthesis and respiration. SA-mediated induction of PR (pathogenesis related) proteins was dependent on the presence of intact photoreceptors, linking light to defense (Karpinski et al., 2003). A connection between SA and photosynthesis is the protein isochorismate synthase, which is involved in SA synthesis, but also in the synthesis of phylloquinone, which is incorporated into photosystem I (Szechynska-Hebda and Karpinski, 2013). An excess excitation energy has similar effects on the expression of nuclear genes involved systemic acquired acclimation and systemic acquired resistance, which are both tightly linked to programmed cell death (reviewed in Szechynska-Hebda and Karpinski, 2013). However, recently we have shown that auxin and SA systemically co-increased during infection of Arabidopsis thaliana with Cucumber mosaic virus (Likić et al., 2014), so that not in all cases an antagonism of auxin and SA can be anticipated.
When talking about “auxin” the major compounds in plants, indole-3-acetic acid (IAA) is usually meant, but there are some indole and other derivatives with auxin activity (Epstein and Ludwig-Müller, 1993, Ludwig-Müller, 2000, Ludwig-Müller and Cohen, 2002). Also, only the free form of IAA and related compounds is considered to be active, the majority of auxin in a given tissue, however, is conjugated mainly to amino acids and sugars and thereby inactivated (Ludwig-Müller, 2011). Since IAA can be even growth inhibitory at high concentrations, the tight control of auxin homeostasis is essential. Here, several processes are important: (1) biosynthesis, (2) degradation, (3) reversible conjugation, and (4) transport, the latter includes long distance and cell-to-cell movement of auxin, leading to local auxin maxima or auxin gradients (e.g. Smith, 2008). These four main possibilities to control auxin concentrations in a given tissue are connected to transcriptional activation of auxin-inducible genes, which can be growth or defense related (Fig. 1). In the case of expansins the proteins can act in developmental responses, for example cell expansion, or in changing the penetration environment (cell wall) for pathogens.
In addition to developmental processes, IAA has come into focus to play a role in plant defense processes against pathogens, mainly bacteria and fungi. In some cases the pathogens use the auxin machinery to induce disease symptoms (Fig. 1), such as crown gall disease (Gelwin, 1990) or clubroots (Ludwig-Müller et al., 2009b). In other instances, they highjack the auxin signaling or conjugation pathways in their own favor to manipulate plant defense responses (Fig. 2, Fig. 3). Finally, there are some examples where auxins could be directly inhibitory and thus involved in the defense response of the plant (Fig. 3). These examples show that the benefit for a plant can be turned against it by pathogens, but vice versa the pathogens can be fought off as well (Table 1). Some examples indicative of the above dilemma will be discussed for plant–pathogens from diverse evolutionary groups to demonstrate the use of similar strategies among different organisms, but also how variable such strategies can turn out.
On the other hand there are plant growth promoting soil microbes either producing IAA (Patten and Glick, 2002), or mediating the IAA levels in the plants (Fig. 1). The growth promoting basidiomycete Piriformospora indica has been shown to produce auxin in culture (Sirrenberg et al., 2007, Vadassery et al., 2008), but the contribution of IAA to the growth promotion phenotype of colonized plants is still a matter of debate. Only recent work has reported that P. indica uses the auxin biosynthesis pathway via tryptamine as an intermediate (Hilbert et al., 2012). It was also shown that a gene encoding one protein from the pathway was expressed during the biotrophic phase of the interaction. However, attenuation of IAA synthesis in a transgenic fungus did not have an effect on growth promotion (Hilbert et al., 2012), confirming earlier results (Vadassery et al., 2008). Addition of low IAA concentrations led to suppression of an oxidative burst in barley, suggesting that the IAA produced by the fungus could interfere/suppress host plant defense (Hilbert et al., 2012, Hilbert et al., 2013). For arbuscular mycorrhiza it has been shown that two auxin might play a role, IAA and indole-3-butyric acid (IBA) (Ludwig-Müller et al., 1997, Kaldorf and Ludwig-Müller, 2000). Auxin could be involved in the mediation of the root phenotype seen in some species, i.e. more lateral roots in mycorrhized plants of maize (Kaldorf and Ludwig-Müller, 2000). In the rhizobium–legume interaction also some indications have been published that IAA is needed for the initiation of the root nodules as organs, especially the intact auxin transport machinery (Wasson et al., 2006). Also, Campanella et al. (2008) have shown that some members of an auxin conjugate hydrolase family from Medicago truncatula were transcriptionally upregulated both during arbusuclar mycorrhiza formation and nodulation, which could lead to higher free IAA levels. While these are examples for the beneficial role of auxin in plant–microbe interactions, in the following different strategies of plant–pathogens will be specifically discussed.
Section snippets
Auxin biosynthesis
Auxin biosynthesis can contribute to the symptoms of certain plant diseases, but is also essential for the normal development of the plant and its orientation in the environment. Either a pathogen highjacks the biosynthetic system of the host plant, or it can produce the auxin itself. One prominent example for the latter is the tumor formation induced by the soil bacterium Agrobacterium tumefaciens, where genes for auxin and cytokinin biosynthesis are stably transformed into the plant tissue (
Auxin signaling and transport
Auxin signaling is central to many plant–pathogen interactions. Therefore, modulation of the signaling pathway is a hallmark for many pathogenic organisms (for detailed review see Fu and Wang, 2011). The role of auxin in plant susceptibility to microbes was first demonstrated in A. thaliana when miR393-mediated down-regulation of auxin receptors (TIR1, AFB1-3) led to the suppression of auxin signaling and to a higher resistance of the plant (Navarro et al., 2006). Later, Navarro et al. (2008)
Auxin homeostasis
While the level of free (active) auxin is controlled by several mechanisms (biosynthesis and transport also belong to them), auxin homeostasis is mainly defined as the binding of free auxin to small or large molecules as inactive auxin conjugates and the reversible hydrolysis which yields again the active hormone. Auxin conjugate synthetases of the GH3 family and auxin amino acid conjugate hydrolases (short auxin amidohydrolases) are the enzymes involved in these processes (reviewed in
Conclusion
In this review some aspects on the dual roles of the plant hormone auxin in plant defense mechanisms and in plant developmental processes have been discussed. Under non-stress conditions the concentration of IAA needs to be tightly controlled to ensure that growth is not limited by either too low or too high auxin levels. This can be achieved by various processes, such as biosynthesis, degradation, transport or reversible inactivation (Fig. 1). Also, control of auxin-induced gene expression is
Acknowledgements
Work in the authors laboratory was supported by the European Union, the State of Saxony, and the Deutsche Forschungsgemeinschaft. This paper is a joint effort of the corresponding authors and an outcome of a workshop kindly supported by sDiv, the Synthesis Centre of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig (DFG FZT 118).
References (78)
Implication of evolution and diversity in arbuscular and ectomycorrhizal symbioses
J Plant Physiol
(2015)- et al.
Indole derivatives produced by the fungus Colletotrichum acutatum causing lime anthracnose and postbloom fruit drop of citrus
FEMS Microbiol Lett
(2003) Camalexin
Phytochemistry
(2007)- et al.
The value of biodiversity in legume symbiotic nitrogen fixation and nodulation for biofuel and food production
J Plant Physiol
(2015) - et al.
Lateral root formation and patterning in Medicago truncatula
J Plant Physiol
(2014) - et al.
Light perception in plant disease defence signalling
Curr Opin Plant Biol
(2003) - et al.
Linking development to defense: auxin in plant–pathogen interactions
Trends Plant Sci
(2009) - et al.
Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi
Mol Plant
(2008) - et al.
Controlling hormone signaling is a plant and pathogen challenge for growth and survival
Curr Opin Plant Biol
(2008) - et al.
Indole-3-butyric acid (IBA) is enhanced in young maize (Zea mays L.) roots colonized with the arbuscular mycorrhizal fungus Glomus intraradices
Plant Sci
(1997)
Arabidopsis plants transformed with nitrilase 1 or 2 in antisense direction are delayed in clubroot development
J Plant Physiol
Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate
J Biol Chem
Flavonoids and auxin transport: modulators or regulators?
Trends Plant Sci
Light intensity-dependent retrograde signalling in higher plants
J Plant Physiol
Biocontrol of Botrytis cinerea in apple fruit by Cryptococcus laurentii and indole-3-acetic acid
Biol Control
Exploiting natural genetic diversity and mutant resources of Arabidopsis thaliana to study the A. thaliana–Plasmodiophora brassicae interaction
Plant Breed
Plants versus pathogens: an evolutionary arms race
Funct Plant Biol
Two potential indole-3-acetaldehyde dehydrogenases in the phytopathogenic fungus Ustilago maydis
Eur J Biochem
Cell wall degradation by Taphrina deformans in host leaf cells
Mycopathologia
Indolic glucosinolates at the crossroads of tryptophan metabolism
Phytochem Rev
The auxin conjugate hydrolase family of Medicago truncatula and their expression during the interaction with two symbionts
J Plant Growth Regul
Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology
Proc Natl Acad Sci USA
The growing world of expansins
Plant Cell Physiol
The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover
Plant Physiol
Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs
Front Plant Sci
Plant hormones: a key in clubroot development
Commun Agric Appl Biol Sci
A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis
Mol Plant–Microbe Interact
Activation of the indole-3-acetic acid–amido synthetase gh3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice
Plant Cell
Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport
Physiol Plant
Insights into auxin signaling in plant–pathogen interactions
Frontiers Plant Sci
Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice
Plant Physiol
Crown gall disease and hairy root disease
Plant Physiol
BIG: a calossin-like protein required for polar auxin transport in Arabidopsis
Genes Dev
The conjugated auxin indole-3-acetic acid-aspartic acid promotes plant disease development
Plant Cell
Expression and localization of nitrilase during symptom development of the clubroot disease in Arabidopsis thaliana
Plant Physiol
Is pathogenicity of Ustilago maydis (huitlacoche) strains on maize related to in vitro production of indole-3-acetic acid?
World J Microbiol Biotechnol
Biology and biochemistry of glucosinolates
Annu Rev Plant Biol
Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots
New Phytol
Cited by (115)
Illuminating the signalomics of microbial biofilm on plant surfaces
2023, Biocatalysis and Agricultural BiotechnologyRecent Advances in Dissecting the Function of Ethylene in Interaction between Host and Pathogen
2024, Journal of Agricultural and Food Chemistry
- ☆
This article is part of a Special Issue entitled: Plant Physiology meets Biodiversity.