Growth-defense Tradeoffs Research Articles

It takes two to tango – molecular links between plant immunity and brassinosteroid signalling

In response to the invasion of microorganisms, plants actively balance their resources for growth and defence, thus ensuring their survival. The regulatory mechanisms underlying plant immunity and growth operate through complex networks, in which the brassinosteroid phytohormone is one of the central players. In the past decades, a growing number of studies have revealed a multi-layered crosstalk between brassinosteroid-mediated growth and plant immunity. In this Review, by means of the tango metaphor, we immerse ourselves into the intimate relationship between brassinosteroid and plant immune signalling pathways that is tailored by the lifestyle of the pathogen and modulated by other phytohormones. The plasma membrane is the unique stage where brassinosteroid and immune signals are dynamically integrated and where compartmentalization into nanodomains that host distinct protein consortia is crucial for the dance. Shared downstream signalling components and transcription factors relay the tango play to the nucleus to activate the plant defence response and other phytohormonal signalling pathways for the finale. Understanding how brassinosteroid and immune signalling pathways are integrated in plants will help develop strategies to minimize the growth-defence trade-off, a key challenge for crop improvement.

The Molecular Priming of Defense Responses is Differently Regulated in Grapevine Genotypes Following Elicitor Application against Powdery Mildew.

Molecular changes associated with response to powdery mildew (PM) caused by Erysiphe necator have been largely explored in Vitis vinifera cultivars, but little is known on transcriptional and metabolic modifications following application of resistance elicitors against this disease. In this study, the whole transcriptome sequencing, and hormone and metabolite analyses were combined to dissect long-term defense mechanisms induced by molecular reprogramming events in PM-infected ‘Moscato’ and ‘Nebbiolo’ leaves treated with three resistance inducers: acibenzolar-S-methyl, potassium phosphonate, and laminarin. Although all compounds were effective in counteracting the disease, acibenzolar-S-methyl caused the most intense transcriptional modifications in both cultivars. These involved a strong down-regulation of photosynthesis and energy metabolism and changes in carbohydrate accumulation and partitioning that most likely shifted the plant growth-defense trade-off towards the establishment of disease resistance processes. It was also shown that genotype-associated metabolic signals significantly affected the cultivar defense machinery. Indeed, ‘Nebbiolo’ and ‘Moscato’ built up different defense strategies, often enhanced by the application of a specific elicitor, which resulted in either reinforcement of early defense mechanisms (e.g., epicuticular wax deposition and overexpression of pathogenesis-related genes in ‘Nebbiolo’), or accumulation of endogenous hormones and antimicrobial compounds (e.g., high content of abscisic acid, jasmonic acid, and viniferin in ‘Moscato’).

CYP20-3 deglutathionylates 2-CysPRX A and suppresses peroxide detoxification during heat stress.

In plants, growth-defense trade-offs occur because of limited resources, which demand prioritization towards either of them depending on various external and internal factors. However, very little is known about molecular mechanisms underlying their occurrence. Here, we describe that cyclophilin 20-3 (CYP20-3), a 12-oxo-phytodienoic acid (OPDA)-binding protein, crisscrosses stress responses with light-dependent electron reactions, which fine-tunes activities of key enzymes in plastid sulfur assimilations and photosynthesis. Under stressed states, OPDA, accumulates in the chloroplasts, binds and stimulates CYP20-3 to convey electrons towards serine acetyltransferase 1 (SAT1) and 2-Cys peroxiredoxin A (2CPA). The latter is a thiol-based peroxidase, protecting and optimizing photosynthesis by reducing its toxic byproducts (e.g., H2O2). Reduction of 2CPA then inactivates its peroxidase activity, suppressing the peroxide detoxification machinery, whereas the activation of SAT1 promotes thiol synthesis and builds up reduction capacity, which in turn triggers the retrograde regulation of defense gene expressions against abiotic stress. Thus, we conclude that CYP20-3 is a unique metabolic hub conveying resource allocations between plant growth and defense responses (trade-offs), ultimately balancing optimal growth phonotype.

Climate drives intraspecific differentiation in the expression of growth-defence trade-offs in a long-lived pine species

Intraspecific variation in plant defences is expected to be the result of adaptive and plastic responses to environmental conditions, where trade-offs between growth and defences are thought to play a key role shaping phenotypic patterns in defensive investment. Axial resin ducts are costly defensive structures that remain imprinted in the tree rings of conifers, therefore being a valuable proxy of defensive investment along the trees’ lifespan. We aimed to disentangle climate-driven adaptive clines and plastic responses to both spatial and temporal environmental variation in resin duct production, and to explore growth-defence trade-offs. To that aim, we applied dendrochronological procedures to quantify annual growth and resin duct production during a 31-year-period in a Mediterranean pine species, including trees from nine populations planted in two common gardens. Both genetic factors and plastic responses modulated annual resin duct production. However, we found no evidence of adaptive clines with climate gradients driving population differentiation. Our results revealed a marked physiological trade-off between growth and defences, where the slope of the trade-off was genetically variable and associated with climatic gradients. Our results help to enlighten the evolutionary patterns and genetic basis of defensive allocation within species, particularly revealing a key role of growth-defence trade-offs.

MYB43 in Oilseed Rape (Brassica napus) Positively Regulates Vascular Lignification, Plant Morphology and Yield Potential but Negatively Affects Resistance to Sclerotinia sclerotiorum.

Arabidopsis thaliana MYB43 (AtMYB43) is suggested to be involved in cell wall lignification. PtrMYB152, the Populus orthologue of AtMYB43, is a transcriptional activator of lignin biosynthesis and vessel wall deposition. In this research, MYB43 genes from Brassica napus (rapeseed) and its parental species B. rapa and B. oleracea were molecularly characterized, which were dominantly expressed in stem and other vascular organs and showed responsiveness to Sclerotinia sclerotiorum infection. The BnMYB43 family was silenced by RNAi, and the transgenic rapeseed lines showed retardation in growth and development with smaller organs, reduced lodging resistance, fewer silique number and lower yield potential. The thickness of the xylem layer decreased by 28%; the numbers of sclerenchymatous cells, vessels, interfascicular fibers, sieve tubes and pith cells in the whole cross section of the stem decreased by 28%, 59%, 48%, 34% and 21% in these lines, respectively. The contents of cellulose and lignin decreased by 17.49% and 16.21% respectively, while the pectin content increased by 71.92% in stems of RNAi lines. When inoculated with S. sclerotiorum, the lesion length was drastically decreased by 52.10% in the stems of transgenic plants compared with WT, implying great increase in disease resistance. Correspondingly, changes in the gene expression patterns of lignin biosynthesis, cellulose biosynthesis, pectin biosynthesis, cell cycle, SA- and JA-signals, and defensive pathways were in accordance with above phenotypic modifications. These results show that BnMYB43, being a growth-defense trade-off participant, positively regulates vascular lignification, plant morphology and yield potential, but negatively affects resistance to S. sclerotiorum. Moreover, this lignification activator influences cell biogenesis of both lignified and non-lignified tissues of the whole vascular organ.

Plant ontogeny determines strength and associated plant fitness consequences of plant-mediated interactions between herbivores and flower visitors.

Plants show ontogenetic variation in growth–defence strategies to maximize reproductive output within a community context. Most work on plant ontogenetic variation in growth–defence trade‐offs has focussed on interactions with antagonistic insect herbivores. Plants respond to herbivore attack with phenotypic changes. Despite the knowledge that plant responses to herbivory affect plant mutualistic interactions with pollinators required for reproduction, indirect interactions between herbivores and pollinators have not been included in the evaluation of how ontogenetic growth–defence trajectories affect plant fitness.In a common garden experiment with the annual Brassica nigra, we investigated whether exposure to various herbivore species on different plant ontogenetic stages (vegetative, bud or flowering stage) affects plant flowering traits, interactions with flower visitors and results in fitness consequences for the plant.Effects of herbivory on flowering plant traits and interactions with flower visitors depended on plant ontogeny. Plant exposure in the vegetative stage to the caterpillar Pieris brassicae and aphid Brevicoryne brassicae led to reduced flowering time and flower production, and resulted in reduced pollinator attraction, pollen beetle colonization, total seed production and seed weight. When plants had buds, infestation by most herbivore species tested reduced flower production and pollen beetle colonization. Pollinator attraction was either increased or reduced. Plants infested in the flowering stage with P. brassicae or Lipaphis erysimi flowered longer, while infestation by any of the herbivore species tested increased the number of flower visits by pollinators.Our results show that the outcome of herbivore–flower visitor interactions in B. nigra is specific for the combination of herbivore species and plant ontogenetic stage. Consequences of herbivory for flowering traits and reproductive output were strongest when plants were attacked early in life. Such differences in selection pressures imposed by herbivores to specific plant ontogenetic stages may drive the evolution of distinct ontogenetic trajectories in growth–defence–reproduction strategies and include indirect interactions between herbivores and flower visitors. Synthesis. Plant ontogeny can define the direct and indirect consequences of herbivory. Our study shows that the ontogenetic stage of plant individuals determined the effects of herbivory on plant flowering traits, interactions with flower visitors and plant fitness.

A Phytochrome B-Independent Pathway Restricts Growth at High Levels of Jasmonate Defense.

The plant hormone jasmonate (JA) promotes resistance to biotic stress by stimulating the degradation of JASMONATE ZIM-DOMAIN (JAZ) proteins, which relieves repression on MYC transcription factors that execute defense programs. JA-triggered depletion of JAZ proteins in Arabidopsis (Arabidopsis thaliana) is also associated with reduced growth and seed production, but the mechanisms underlying these pleiotropic growth effects remain unclear. Here, we investigated this question using an Arabidopsis JAZ-deficient mutant (jazD; jaz1-jaz7, jaz9, jaz10, and jaz 13) that exhibits high levels of defense and strong growth inhibition. Genetic suppressor screens for mutations that uncouple growth-defense tradeoffs in the jazD mutant identified nine independent causal mutations in the red-light receptor phytochrome B (phyB). Unlike the ability of the phyB mutations to completely uncouple the mild growth-defense phenotypes in a jaz mutant (jazQ) defective in JAZ1, JAZ3, JAZ4, JAZ9, and JAZ10, phyB null alleles only weakly alleviated the growth and reproductive defects in the jazD mutant. phyB-independent growth restriction of the jazD mutant was tightly correlated with upregulation of the Trp biosynthetic pathway but not with changes in central carbon metabolism. Interestingly, jazD and jazD phyB plants were insensitive to a chemical inhibitor of Trp biosynthesis, which is a phenotype previously observed in plants expressing hyperactive MYC transcription factors that cannot bind JAZ repressors. These data provide evidence that the mechanisms underlying JA-mediated growth-defense balance depend on the level of defense, and they further establish an association between growth inhibition at high levels of defense and dysregulation of Trp biosynthesis.

Root Development and Stress Tolerance in rice: The Key to Improving Stress Tolerance without Yield Penalties.

Roots anchor plants and take up water and nutrients from the soil; therefore, root development strongly affects plant growth and productivity. Moreover, increasing evidence indicates that root development is deeply involved in plant tolerance to abiotic stresses such as drought and salinity. These findings suggest that modulating root growth and development provides a potentially useful approach to improve plant abiotic stress tolerance. Such targeted approaches may avoid the yield penalties that result from growth–defense trade-offs produced by global induction of defenses against abiotic stresses. This review summarizes the developmental mechanisms underlying root development and discusses recent studies about modulation of root growth and stress tolerance in rice.

The versatile functions of OsALDH2B1 provide a genic basis for growth–defense trade-offs in rice

In plants, enhanced defense often compromises growth and development, which is regarded as trade-offs between growth and defense. Here we identified a gene, OsALDH2B1, that functions as a master regulator of the growth-defense trade-off in rice. OsALDH2B1 has its primary function as an aldehyde dehydrogenase and a moonlight function as a transcriptional regulator. Loss of function of OsALDH2B1 greatly enhanced resistance to broad-spectrum pathogens, including fungal blast, bacterial leaf blight, and leaf streak, but caused severe phenotypic changes such as male sterility and reduced plant size, grain size, and number. We showed that its primary function as a mitochondrial aldehyde dehydrogenase conditions male fertility. Its moonlight function of transcriptional regulation, featuring both repressing and activating activities, regulates a diverse range of biological processes involving brassinolide, G protein, jasmonic acid, and salicylic acid signaling pathways. Such regulations cause large impacts on the morphology and immunity of rice plants. The versatile functions of OsALDH2B1 provide an example of the genic basis of growth-defense trade-offs in plants.

Systematic identification of genes associated with plant growth-defense tradeoffs under JA signaling in Arabidopsis.

Co-expression and regulatory networks yield important insights into the growth-defense tradeoffs mechanism under jasmonic acid (JA) signals in Arabidopsis. Elevated defense is commonly associated with growth inhibition. However, a comprehensive atlas of the genes associated with the plant growth-defense tradeoffs under JA signaling is lacking. To gain an insight into the dynamic architecture of growth-defense tradeoffs, a coexpression network analysis was employed on publicly available high-resolution transcriptomes of Arabidopsis treated with coronatine (COR), a mimic of jasmonoyl-l-isoleucine. The genes involved in JA-mediated growth-defense tradeoffs were systematically revealed. Promoter enrichment analysis revealed the core regulatory module in which the genes underwent rapid activation, sustained upregulation after COR treatment, and mediated the growth-defense tradeoffs. Several transcription factors (TFs), including RAP2.6L, MYB44, WRKY40, and WRKY18, were identified as instantly activated components associated with pathogen and insect resistance. JA might rapidly activate RAV1 and KAN1 to repress brassinosteroid (BR) response genes, upregulate KAN1, the C2H2 TF families ZF2, ZF3, ZAT6, and STZ/ZAT10 to repress the biosynthesis, transport, and signaling of auxin to arrest growth. Independent datasets and preserved analyses validated the reproducibility of the results. Our study provided a comprehensive snapshot of genes that respond to JA signals and provided valuable resources for functional studies on the genetic modification of breeding population that exhibit robust growth and defense simultaneously.

Brassinosteroids Antagonize Jasmonate-Activated Plant Defense Responses through BRI1-EMS-SUPPRESSOR1 (BES1).

Brassinosteroids (BRs) and jasmonates (JAs) regulate plant growth, development, and defense responses, but how these phytohormones mediate the growth-defense tradeoff is unclear. Here, we identified the Arabidopsis (Arabidopsis thaliana) dwarf at early stages1 (dwe1) mutant, which exhibits enhanced expression of defensin genes PLANT DEFENSIN1.2a (PDF1.2a) and PDF1.2b The dwe1 mutant showed increased resistance to herbivory by beet armyworms (Spodoptera exigua) and infection by botrytis (Botrytis cinerea). DWE1 encodes ROTUNDIFOLIA3, a cytochrome P450 protein essential for BR biosynthesis. The JA-inducible transcription of PDF1.2a and PDF1.2b was significantly reduced in the BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 (BES1) gain-of-function mutant bes1- D, which was highly susceptible to S. exigua and B. cinerea BES1 directly targeted the terminator regions of PDF1.2a/PDF1.2b and suppressed their expression. PDF1.2a overexpression diminished the enhanced susceptibility of bes1- D to B. cinerea but did not improve resistance of bes1- D to S. exigua In response to S. exigua herbivory, BES1 inhibited biosynthesis of the JA-induced insect defense-related metabolite indolic glucosinolate by interacting with transcription factors MYB DOMAIN PROTEIN34 (MYB34), MYB51, and MYB122 and suppressing expression of genes encoding CYTOCHROME P450 FAMILY79 SUBFAMILY B POLYPEPTIDE3 (CYP79B3) and UDP-GLUCOSYL TRANSFERASE 74B1 (UGT74B1). Thus, BR contributes to the growth-defense tradeoff by suppressing expression of defensin and glucosinolate biosynthesis genes.

Overexpression of native Musa-miR397 enhances plant biomass without compromising abiotic stress tolerance in banana

Plant micro RNAs (miRNAs) control growth, development and stress tolerance but are comparatively unexplored in banana, whose cultivation is threatened by abiotic stress and nutrient deficiencies. In this study, a native Musa-miR397 precursor harboring 11 copper-responsive GTAC motifs in its promoter element was identified from banana genome. Musa-miR397 was significantly upregulated (8–10) fold in banana roots and leaves under copper deficiency, correlating with expression of root copper deficiency marker genes such as Musa-COPT and Musa-FRO2. Correspondingly, target laccases were significantly downregulated (>−2 fold), indicating miRNA-mediated silencing for Cu salvaging. No significant expression changes in the miR397-laccase module were observed under iron stress. Musa-miR397 was also significantly upregulated (>2 fold) under ABA, MV and heat treatments but downregulated under NaCl stress, indicating universal stress-responsiveness. Further, Musa-miR397 overexpression in banana significantly increased plant growth by 2–3 fold compared with wild-type but did not compromise tolerance towards Cu deficiency and NaCl stress. RNA-seq of transgenic and wild type plants revealed modulation in expression of 71 genes related to diverse aspects of growth and development, collectively promoting enhanced biomass. Summing up, our results not only portray Musa-miR397 as a candidate for enhancing plant biomass but also highlight it at the crossroads of growth-defense trade-offs.

Rhizosphere-Associated Pseudomonas Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH

The root microbiome consists of commensal, pathogenic, and plant-beneficial microbes [1]. Most members of the root microbiome possess microbe-associated molecular patterns (MAMPs) similar to those of plant pathogens [2]. Their recognition can lead to the activation of host immunity and suppression of plant growth due to growth-defensetradeoffs [3, 4]. We found that 42% of the tested root microbiota, including the plant growth-promoting rhizobacteria Pseudomonas capeferrum WCS358 [5, 6] and Pseudomonas simiae WCS417 [6, 7], are able to quench local Arabidopsis thaliana root immune responses that aretriggered by flg22 [8], an immunogenic epitope of the MAMP flagellin [9], suggesting that this is animportant function of the root microbiome. Ina screen for WCS358 mutants that lost their capacity to suppress flg22-induced CYP71A12pro:GUS MAMP-reporter gene expression, we identified the bacterial genes pqqF and cyoB in WCS358, which are required for the production of gluconic acid and its derivative 2-keto gluconic acid. Both WCS358 mutants are impaired in the production of these organic acids and consequently lowered their extracellular pH to a lesser extent thanwild-type WCS358. Acidification of the plant growth medium similarly suppressed flg22-induced CYP71A12pro:GUS and MYB51pro:GUS expression, and the flg22-mediated oxidative burst, suggesting a role for rhizobacterial gluconic acid-mediated modulation of the extracellular pH in the suppression of root immunity. Rhizosphere population densities of the mutants were significantly reduced compared to wild-type. Collectively, these findings show thatsuppression of immune responses is an important function of the root microbiome, as it facilitates colonization by beneficial root microbiota.

A growth-defense trade-off is general across native and exotic grasses.

High-resource environments typically favor quick-growing, poorly defended plants, while resource-poor environments typically favor slow-growing, well-defended plants. The prevailing hypothesis explaining this pattern states that, as resource availability increases, well-defended, slow-growing species are replaced by poorly defended, fast-growing species. A second hypothesis states that greater resource availability increases allocation to growth at the expense of defense, within species. Regardless of mechanism, if exotic species are released from enemies relative to natives, shifts in allocation to growth and defense both within and among species could differ by geographic provenance. To test whether resource availability alters growth or defense, within and among species, and whether any such effects differ between natives and exotics, we manipulated soil nutrient supply and access of aboveground insect herbivores and fungal pathogens under field conditions to individuals of six native and six exotic grass species that co-occurred in a North Carolina old field. The prevailing hypothesis' prediction-that species-level enemy impact increases with species' nutrient responsiveness-was confirmed. Moreover, this relationship did not differ between native and exotic species. The second hypothesis' prediction-that individual-level enemy impact increases with nutrient supply, after accounting for species-level variation in performance-was not supported. Together, these results support the idea, across native and exotic species, that plant species turnover is the primary mechanism underlying effects of nutrient enrichment on allocation to growth and defense in plant communities.

Root-associated microorganisms reprogram plant life history along the growth-stress resistance tradeoff.

Growth-defense tradeoffs are a major constraint on plant evolution. While the genetics of resource allocation is well established, the regulatory role of plant-associated microorganisms is still unclear. Here, we demonstrate that plant-associated microorganisms can reposition the plant phenotype along the same growth-defense tradeoff that determines phenotypic effects of plant mutations. We grew plants with microorganisms altering ethylene balance, a key hormone regulating plant investment into growth and stress tolerance. Microbial ethylene reduction had a similar effect to mutations disrupting ethylene signaling: both increased plant growth but at the cost of a strong stress hypersensitivity. We conclude that microbial impact on phenotype can offset the effects of mutations and that apparent plant growth promotion has strong pleiotropic effects. This study confirms that plant life history should be addressed as a joint product of plant genotype and its associated microbiota.

Unraveling the Genetic Elements Involved in Shoot and Root Growth Regulation by Jasmonate in Rice Using a Genome-Wide Association Study

BackgroundDue to their sessile life style, plant survival is dependent on the ability to build up fast and highly adapted responses to environmental stresses by modulating defense response and organ growth. The phytohormone jasmonate plays an essential role in regulating these plant responses to stress.ResultsTo assess variation of plant growth responses and identify genetic determinants associated to JA treatment, we conducted a genome-wide association study (GWAS) using an original panel of Vietnamese rice accessions. The phenotyping results showed a high natural genetic variability of the 155 tested rice accessions in response to JA for shoot and root growth. The level of growth inhibition by JA is different according to the rice varieties tested. We conducted genome-wide association study and identified 28 significant associations for root length (RTL), shoot length (SHL), root weight (RTW), shoot weight (SHW) and total weight (TTW) in response to JA treatment. Three common QTLs were found for RTL, RTW and SHL. Among a list of 560 candidate genes found to co-locate with the QTLs, a transcriptome analysis from public database for the JA response allows us to identify 232 regulated genes including several JA-responsive transcription factors known to play a role in stress response.ConclusionOur genome-wide association study shows that common and specific genetic elements are associated with inhibition of shoot and root growth under JA treatment suggesting the involvement of a complex JA-dependent genetic control of rice growth inhibition at the whole plant level. Besides, numerous candidate genes associated to stress and JA response are co-located with the association loci, providing useful information for future studies on genetics and breeding to optimize the growth-defense trade-off in rice.

Beneficial microbes going underground of root immunity.

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe‐associated molecular patterns (MAMPs). However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root‐invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free‐living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root‐invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth‐defense tradeoffs triggered by the MAMP‐rich rhizosphere environment.

DELLA and EDS1 Form a Feedback Regulatory Module to Fine-Tune Plant Growth–Defense Tradeoff in Arabidopsis

Plants maintain a dynamic balance between growth and defense , and optimize allocation of resources for survival under constant pathogen infections. However, the underlying molecular regulatory mechanisms, especially in response to biotrophic bacterial infection, remain elusive. Here, we demonstrate that DELLA proteins and EDS1, an essential resistance regulator, form a central module modulating plant growth–defense tradeoffs via direct interaction. When infected by Pst DC3000, EDS1 rapidly promotes salicylic acid (SA) biosynthesis and resistance-related gene expression to prime defense response, while pathogen infection stabilizes DELLA proteins RGA and RGL3 to restrict growth in a partially EDS1-dependent manner, which facilitates plants to develop resistance to pathogens. However, the increasingly accumulated DELLAs interact with EDS1 to suppress SA overproduction and excessive resistance response. Taken together, our findings reveal a DELLA–EDS1-mediated feedback regulatory loop by which plants maintain the subtle balance between growth and defense to avoid excessive growth or defense in response to constant biotrophic pathogen attack.

Plant-Beneficial <i>Pseudomonas</i> Spp. Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH

The plant root microbiome consists of commensal, pathogenic and plant-beneficial microbes. Most members of the root microbiome possess microbe-associated molecular patterns (MAMPs) similar to those of plant pathogens. Their recognition by the cell surface-localized pattern recognition receptors can lead to the initiation of host immune signaling and suppression of plant growth due to growth-defense tradeoffs. We found that 42% of the tested root microbiota, including the plant growth-promoting rhizobacteria Pseudomonas capeferrum WCS358 (WCS358) and Pseudomonas simiae WCS417, are able to quench local Arabidopsis thaliana root immune responses that were triggered by the synthetic MAMP flg22, suggesting that this is an important function of the root microbiome. In a screen for WCS358 mutants that lost their capacity to suppress flg22-induced CYP71A12pro:GUS MAMP-reporter gene expression, we identified the bacterial genes pqqF and cyoB in WCS358. CyoB and pqqF are required for the production of gluconic acid and its derivative 2-keto gluconic acid. Both WCS358 mutants are impaired in the production of these organic acids and consequently lowered their extracellular pH to a lesser extent than wild-type WCS358. Acidification of the plant growth medium similarly suppressed flg22-induced CYP71A12pro:GUS and MYB51pro:GUS expression as well as the flg22-mediated oxidative burst, suggesting a role for rhizobacterial gluconic acid-mediated modulation of the extracellular pH in the suppression of local root immunity. Rhizosphere population densities of the mutants were significantly reduced compared to wild-type. Collectively, these findings show that suppression of local root immune responses is an important function of the root microbiome, as it facilitates colonization by beneficial root microbiota.

Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates.

The growth-defense trade-off in plant biology has gained enormous traction in the last two decades, highlighting the importance of understanding how plants deal with two of the greatest challenges for their survival and reproduction. It has been well established that in response to competition signals perceived by informational photoreceptors, shade-intolerant plants typically activate the shade-avoidance syndrome (SAS). In turn, in response to signals of biotic attack, plants activate a suite of defense responses, many of which are directed to minimize the loss of plant tissue to the attacking agent (broadly defined, the defense syndrome, DS). We argue that components of the SAS, including increased elongation, apical dominance, reduced leaf mass per area (LMA), and allocation to roots, are in direct conflict with configurational changes that plants require to maximize defense. We hypothesize that these configurational trade-offs provide a functional explanation for the suppression of components of the DS in response to competition cues. Based on this premise, we discuss recent advances in the understanding of the mechanisms by which informational photoreceptors, by interacting with jasmonic acid (JA) signaling, help the plant to make intelligent allocation and developmental decisions that optimize its configuration in complex biotic contexts.