Growth-defense Tradeoffs Research Articles

Growth–defense trade-offs in plants

Walking through a garden or a crop field, you may notice that plants damaged by pests (insects or pathogens) look smaller than the same kind of plants nearby that are not damaged. An obvious explanation would be that damaged plants may have lost substantial photosynthetic tissue due to insect and pathogen activities. As such, plants may have a reduced ability to capture light and perform photosynthesis, which fuels the growth of plants. While this is likely part of the reason why damaged plants look smaller, there is also another and perhaps more fascinating explanation that we would like to discuss here in this primer. It turns out that plants attacked by insects, pathogens and other biotic stressors may 'purposely' slow down their growth and that this response is often systemic, meaning that it occurs throughout the plant and beyond the tissue that is damaged by pests. Interestingly, some chemicals or plant genetic mutations that simulate insect or pathogen attacks without causing a loss of photosynthetic tissue can also slow plant growth, suggesting the physical loss of photosynthetic tissue per se is not always a prerequisite for slowing down plant growth. In contrast, there are conditions under which plants need to grow rapidly. For example, plants grow quickly when searching for light during germination or under a shaded canopy due to crowding from neighboring plants. Under these conditions, rapid plant growth is often accompanied by increased susceptibility to pests, presumably because growth is prioritized over defense. This inverse growth-defense relationship is commonly known as the 'growth-defense trade-off' and may be considered one of the most fundamental principles of 'plant economics' that allows plants to adjust growth and defense based on external conditions (Figure 1). As plants must both grow and defend in order to reproduce and survive in the natural world, growth-defense trade-offs have important ecological consequences. In agricultural settings, crops have often been bred to maximize growth-related traits, which could inadvertently result in the loss of useful genetic traits for biotic defenses. Thus, deciphering the molecular mechanisms underlying growth-defense trade-off phenomena could impact future crop breeding strategies aimed at designing superior crop plants with high yields as well as the ability to defend against biotic stressors. Here, we discuss some of the prevailing hypotheses about growth-defense trade-offs, our current understanding of the underlying mechanisms, and the ongoing efforts to optimize growth-defense trade-offs in crop plants.

CRISPR-Cas9 helps solve a piece of the puzzle of the biosynthesis of salicinoids and suggests a role in the growth-defense trade-off in poplar.

CRISPR-Cas9 helps solve a piece of the puzzle of the biosynthesis of salicinoids and suggests a role in the growth-defense trade-off in poplar.

Transcriptome analysis revealed that grafting improves the resistance of pepper to Phytophthora capsici by fine-tuning growth-defense tradeoff

DOI 10.15835/nbha50212705
 Grafting has been widely used to defense soil borne diseases and nematodes in vegetables production. However, the underlying mechanism of grafting-improved disease resistance is largely unknown. In this study, grafting cv. ‘Ledu’ scion to cv. ‘Jingxin No. 5’ rootstocks improved the resistance of pepper to Phytophthora capsici. To gain insights into the regulatory networks related to grafting, we performed transcriptome analysis of grafting and control pepper plants with or without P. capsici inoculation. RNA-seq analysis revealed that P. capsici infection largely re-programmed the pepper transcriptome and differentially expressed genes (DEGs) functionally annotated to metabolism processes including photosynthesis, response to stimulus, enzyme activity, and transcription were significantly enriched. Furthermore, the expression levels of most DEGs induced by P. capsici infection, such as genes functionally related to plant hormone signal transduction, plant-pathogen interaction, photosynthesis, reactive oxygen species, tend to recover to the control levels in grafting pepper plants, which help pepper maintain moderate plant defense response and considerable accumulation level of assimilation product, therefore fine-turning the dynamic balance between pepper growth-defense tradeoffs. Taken together, our results suggest the dynamic transcriptional programming in grafting pepper that underpin P. capsici disease and providing insight that the fine-tuning balance between growth and defense of grafting pepper.

Genomics and Pathways Involved in Maize Resistance to Fusarium Ear Rot and Kernel Contamination With Fumonisins.

Fusarium verticillioides is a causal agent of maize ear rot and produces fumonisins, which are mycotoxins that are toxic to animals and humans. In this study, quantitative trait loci (QTLs) and bulk-segregant RNA-seq approaches were used to uncover genomic regions and pathways involved in resistance to Fusarium ear rot (FER) and to fumonisin accumulation in maize kernels. Genomic regions at bins 4.07–4.1, 6–6.01, 6.04–6.05, and 8.05–8.08 were related to FER resistance and/or reduced fumonisin levels in kernels. A comparison of transcriptomes between resistant and susceptible inbred bulks 10 days after inoculation with F. verticillioides revealed 364 differentially expressed genes (DEGs). In the resistant inbred bulks, genes involved in sink metabolic processes such as fatty acid and starch biosynthesis were downregulated, as well as those involved in phytosulfokine signaling and many other genes involved in cell division; while genes involved in secondary metabolism and compounds/processes related to resistance were upregulated, especially those related to cell wall biosynthesis/rearrangement and flavonoid biosynthesis. These trends are indicative of a growth–defense trade-off. Among the DEGs, Zm00001d053603, Zm00001d035562, Zm00001d037810, Zm00001d037921, and Zm00001d010840 were polymorphic between resistant and susceptible bulks, were located in the confidence intervals of detected QTLs, and showed large differences in transcript levels between the resistant and susceptible bulks. Thus, they were identified as candidate genes involved in resistance to FER and/or reduced fumonisin accumulation.

Polyploidy and growth-defense tradeoffs in natural populations of western quaking Aspen.

Polyploidy, the expression of more than two sets of chromosomes, is common in plants, and is thought to influence plant trait expression and drive plant species evolution. The degree to which polyploidy influences interactions among physiological processes such as growth and defense in natural populations through its effect on phenotypic variability is poorly understood. We link broad plant genotypic features (including polyploidy) to phenotypic expression of growth and chemical defense in natural populations of quaking aspen (Populus tremuloides) to examine patterns in resource allocation that might drive growth-defense tradeoffs. Quaking aspen are capable of rapid growth, and are also a primary food plant for a large range of herbivores, including insects and ungulates. While often diploid, aspen can exhibit polyploidy as triploid clones. We tested for the effect of genotype, cytotype (ploidy level, divided between diploids and triploids), and ramet age on relationships between growth and leaf chemistry across natural aspen clones in northern Utah. Substantial genotype variability in growth and leaf chemistry occurred across both cytotypes. Phenolic glycosides, but not condensed tannins, were negatively related to growth. Ramet age was also negatively related to growth. Phenolic glycosides were negatively related to condensed tannins, but only for the diploid clones. Triploid clones exhibited ~ 20% higher levels of phenolic glycosides than diploids. Growth in quaking aspen was likely sacrificed for the production of phenolic glycosides. Our study underscores the importance of considering polyploidy, genetic variability, and ramet age in understanding growth-defense tradeoffs in natural populations of clonal organisms, such as quaking aspen.

Do mitochondria hold the key to understanding growth-defense tradeoffs?

Do mitochondria hold the key to understanding growth-defense tradeoffs?

Genome-wide characterization of the sorghum JAZ gene family and their responses to phytohormone treatments and aphid infestation

Jasmonate ZIM-domain (JAZ) proteins are the key repressors of the jasmonic acid (JA) signal transduction pathway and play a crucial role in stress-related defense, phytohormone crosstalk and modulation of the growth-defense tradeoff. In this study, the sorghum genome was analyzed through genome-wide comparison and domain scan analysis, which led to the identification of 18 sorghum JAZ (SbJAZ) genes. All SbJAZ proteins possess the conserved TIFY and Jas domains and they formed a phylogenetic tree with five clusters related to the orthologs of other plant species. Similarly, evolutionary analysis indicated the duplication events as a major force of expansion of the SbJAZ genes and there was strong neutral and purifying selection going on. In silico analysis of the promoter region of the SbJAZ genes indicates that SbJAZ5, SbJAZ6, SbJAZ13, SbJAZ16 and SbJAZ17 are rich in stress-related cis-elements. In addition, expression profiling of the SbJAZ genes in response to phytohormones treatment (JA, ET, ABA, GA) and sugarcane aphid (SCA) was performed in two recombinant inbred lines (RILs) of sorghum, resistant (RIL 521) and susceptible (RIL 609) to SCA. Taken together, data generated from phytohormone expression and in silico analysis suggests the putative role of SbJAZ9 in JA-ABA crosstalk and SbJAZ16 in JA-ABA and JA-GA crosstalk to regulate certain physiological processes. Notably, upregulation of SbJAZ1, SbJAZ5, SbJAZ13 and SbJAZ16 in resistant RIL during JA treatment and SCA infestation suggests putative functions in stress-related defense and to balance the plant defense to promote growth. Overall, this report provides valuable insight into the organization and functional characterization of the sorghum JAZ gene family.

A Mathematical Model for Characterizing the Biomass and the Physiological/Biochemical Indicators of Salvia miltiorrhiza Based on Growth-Defense Tradeoff.

Carbon(C) and nitrogen(N) metabolisms are important for plant growth and defense, and enzymes play a major role in these two metabolisms. Current studies show that the enzymes of N Metabolism, C Metabolism, and defense are correlated with biomass. Then, we conducted this research under the assumption that enzymes could characterize the relationship based on growth-defense tradeoff, and some of the enzymes could be used to represent the plant growth. From the mechanism model, we picked out 18 physiological/biochemical indicators and obtained the data from 24 tissue culture seedlings of Salvia miltiorrhiza (S.miltiorrhiza) which were grafted with 11 endophytic fungi. Then, the relationship between the biomass and the physiological/biochemical indicators was investigated by using statistical analysis, such as correlation analysis, variable screening, and regression analysis. The results showed that many physiological/biochemical indicators, especially enzyme activities, were related to biomass accumulation. Through a rigorous logical reasoning process, we established a mathematical model of the biomass and 6 key physiological/biochemical indicators, including glutamine synthetase (GS), glutamate synthase (GLS), glutamate dehydrogenase (GDH), peroxidase (POD), catalase (CAT), and soluble protein from Cobb-Douglas production function. This model had high prediction accuracy, and it could simplify the measurement of biomass. During the artificial cultivation of S.miltiorrhiza, we can monitor the biomass accumulation by scaling the key physiological/biochemical indicators in the leaves. Interestingly, the coefficients of Lasso regression during our analysis were consistent with the mechanism of growth-defense tradeoff. Perhaps, the key physiological/biochemical indicators obtained in the statistical analysis are related to the indicators affecting biomass accumulation in practice.

Mycorrhizal symbiosis balances rootstock-mediated growth-defence tradeoffs

Mycorrhizal symbiosis balances rootstock-mediated growth-defence tradeoffs

GT Factor ZmGT-3b Is Associated With Regulation of Photosynthesis and Defense Response to Fusarium graminearum Infection in Maize Seedling.

It is of critical importance for plants to correctly and efficiently allocate their resources between growth and defense to optimize fitness. Transcription factors (TFs) play crucial roles in the regulation of plant growth and defense response. Trihelix TFs display multifaceted functions in plant growth, development, and responses to various biotic and abiotic stresses. In our previous investigation of maize stalk rot disease resistance mechanism, we found a trihelix TF gene, ZmGT-3b, which is primed for its response to Fusarium graminearum challenge by implementing a rapid and significant reduction of its expression to suppress seedling growth and enhance disease resistance. The disease resistance to F. graminearum was consistently increased and drought tolerance was improved, while seedling growth was suppressed and photosynthesis activity was significantly reduced in the ZmGT-3b knockdown seedlings. Thus, the seedlings finally led to show a kind of growth–defense trade-off phenotype. Moreover, photosynthesis-related genes were specifically downregulated, especially ZmHY5, which encodes a conserved central regulator of seedling development and light responses; ZmGT-3b was confirmed to be a novel interacting partner of ZmHY5 in yeast and in planta. Constitutive defense responses were synchronically activated in the ZmGT-3b knockdown seedlings as many defense-related genes were significantly upregulated, and the contents of major cell wall components, such as lignin, were increased in the ZmGT-3b knockdown seedlings. These suggest that ZmGT-3b is involved in the coordination of the metabolism during growth–defense trade-off by optimizing the temporal and spatial expression of photosynthesis- and defense-related genes.

Pulling the strings from underground? Soil biota and plant growth-defense tradeoffs.

This article is a Commentary on Geisen et al. (2022), 233: 1345–1357.

Coordinated resource allocation to plant growth-defense tradeoffs.

Plant resource allocation patterns often reveal tradeoffs that favor growth (G) over defense (D), or vice versa. Ecologists most often explain G-D tradeoffs through principles of economic optimality, in which negative trait correlations are attributed to the reconciliation of fitness costs. Recently, researchers in molecular biology have developed 'big data' resources including multi-omic (e.g. transcriptomic, proteomic and metabolomic) studies that describe the cellular processes controlling gene expression in model species. In this synthesis, we bridge ecological theory with discoveries in multi-omics biology to better understand how selection has shaped the mechanisms of G-D tradeoffs. Multi-omic studies reveal strategically coordinated patterns in resource allocation that are enabled by phytohormone crosstalk and transcriptional signal cascades. Coordinated resource allocation justifies the framework of optimality theory, while providing mechanistic insight into the feedbacks and control hubs that calibrate G-D tradeoff commitments. We use the existing literature to describe the coordinated resource allocation hypothesis (CoRAH) that accounts for balanced cellular controls during the expression of G-D tradeoffs, while sustaining stored resource pools to buffer the impacts of future stresses. The integrative mechanisms of the CoRAH unify the supply- and demand-side perspectives of previous G-D tradeoff theories.

Integrated Application of Transcriptomics and Metabolomics Reveals the Energy Allocation-Mediated Mechanisms of Growth-Defense Trade-Offs in Crassostrea gigas and Crassostrea angulata

Understanding the genetic basis of trait variations and their coordination between relative species or populations distributing in different environmental conditions is important in evolutionary biology. In marine ectotherms, growth-defense trade-offs are a common ecological and evolutionary phenomenon. However, the biochemical and molecular mechanisms that govern these trade-offs in marine ectotherms in the evolutionary perspective remain poorly investigated. Oysters are among the most important species in global aquaculture. Crassostrea gigas (C. gigas) and Crassostrea angulata (C. angulata) are two allopatric congeneric dominant oyster species that inhabit the northern and southern intertidal areas of China. Wild C. gigas and C. angulata were spawned, and their F1 progeny were cultured in the same sites to reduce the environmental effects. Untargeted metabolomics and transcriptomics, together with phenotypic parameters including morphological traits (growth performance), nutritional content (glycogen, crude fat, and fatty acid content), physiology (normalized oxygen consumption rate and total antioxidant capacity) were applied to assess metabolic and transcript divergences between C. gigas and C. angulata. Integrated analyses of metabolites and transcriptomes showed that C. gigas allocated more energy to storage and defense by suppressing glycolysis, fatty acid oxidation and by upregulating fatty acid synthesis, antioxidant gene expression, and related metabolites. The metabolic and transcript results were further confirmed by the phenotypic data that C. gigas has higher glycogen and crude fat content and fatty acid unsaturation and stronger antioxidant capacity than C. angulata. In contrast, C. angulata exhibited better growth performance and a higher oxygen consumption rate. These findings suggest that C. angulata allocates more energy to growth, which is embodied in its stronger aerobic capacity and higher levels of protein synthesis genes, metabolites, and growth-related biomarkers. This study will help to enlighten the evolutionary patterns and genetic basis of growth-defense trade-offs in marine ectotherms and the biochemical and molecular mechanisms underlying energy allocation. Also, the key genes and metabolites of glycogen and fatty acids pathway identified in this study will be applied for meat quality improvement in the oyster industry.

Enhancement of Phytosterol and Triterpenoid Production in Plant Hairy Root Cultures-Simultaneous Stimulation or Competition?

Plant in vitro cultures, including hairy roots, can be applied for controlled production of valuable natural products, such as triterpenoids and sterols. These compounds originate from the common precursor squalene. Sterols and triterpenoids distinctly differ in their functions, and the 2,3-oxidosqualene cyclization step is often regarded as a branch point between primary and secondary (more aptly: general and specialized) metabolism. Considering the crucial role of phytosterols as membrane constituents, it has been postulated that unconstrained biosynthesis of triterpenoids can occur when sterol formation is already satisfied, and these compounds are no longer needed for cell growth and division. This hypothesis seems to follow directly the growth-defense trade-off plant dilemma. In this review, we present some examples illustrating the specific interplay between the two divergent pathways for sterol and triterpenoid biosynthesis appearing in root cultures. These studies were significant for revealing the steps of the biosynthetic pathway, understanding the role of particular enzymes, and discovering the possibility of gene regulation. Currently, hairy roots of many plant species can be considered not only as an efficient tool for production of phytochemicals, but also as suitable experimental models for investigations on regulatory mechanisms of plant metabolism.

Functional modulation of an aquaporin to intensify photosynthesis and abrogate bacterial virulence in rice.

Plant aquaporins are a recently noted biological resource with a great potential to improve crop growth and defense traits. Here, we report the functional modulation of the rice (Oryza sativa) aquaporin OsPIP1;3 to enhance rice photosynthesis and grain production and to control bacterial blight and leaf streak, the most devastating worldwide bacterial diseases in the crop. We characterize OsPIP1;3 as a physiologically relevant CO2 -transporting facilitator, which supports 30% of rice photosynthesis on average. This role is nullified by interaction of OsPIP1;3 with the bacterial protein Hpa1, an essential component of the Type III translocon that supports translocation of the bacterial Type III effectors PthXo1 and TALi into rice cells to induce leaf blight and streak, respectively. Hpa1 binding shifts OsPIP1;3 from CO2 transport to effector translocation, aggravates bacterial virulence, and blocks rice photosynthesis. On the contrary, the external application of isolated Hpa1 to rice plants effectively prevents OsPIP1;3 from interaction with Hpa1 secreted by the bacteria that are infecting the plants. Blockage of the OsPIP1;3-Hpa1 interaction reverts OsPIP1;3 from effector translocation to CO2 transport, abrogates bacterial virulence, and meanwhile induces defense responses in rice. These beneficial effects can combine to enhance photosynthesis by 29-30%, reduce bacterial disease by 58-75%, and increase grain yield by 11-34% in different rice varieties investigated in small-scale field trials conducted during the past years. Our results suggest that crop productivity and immunity can be coordinated by modulating the physiological and pathological functions of a single aquaporin to break the growth-defense tradeoff barrier.

Growth–defense trade-offs shape population genetic composition in an iconic forest tree species

All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a pivotal conflict occurs between allocation to growth, which accelerates resource acquisition, and to defense, which protects existing tissue against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of plant evolutionary ecology is that context-dependence of these trade-offs contributes to the maintenance of intraspecific variation in defense [Züst and Agrawal, Annu. Rev. Plant Biol., 68, 513-534 (2017)]. This prediction has rarely been tested, however, and the evolutionary consequences of growth-defense trade-offs in different environments are poorly understood, especially in long-lived species [Cipollini et al., Annual Plant Reviews (Wiley, 2014), pp. 263-307]. Here we show that intraspecific trait trade-offs, even when fixed across divergent environments, interact with competition to drive natural selection of tree genotypes corresponding to their growth-defense phenotypes. Our results show that a functional trait trade-off, when coupled with environmental variation, causes real-time divergence in the genetic architecture of tree populations in an experimental setting. Specifically, competitive selection for faster growth resulted in dominance by fast-growing tree genotypes that were poorly defended against natural enemies. This outcome is a signature example of eco-evolutionary dynamics: Competitive interactions affected microevolutionary trajectories on a timescale relevant to subsequent ecological interactions [Brunner et al., Funct. Ecol. 33, 7-12 (2019)]. Eco-evolutionary drivers of tree growth and defense are thus critical to stand-level trait variation, which structures communities and ecosystems over expansive spatiotemporal scales.

Beyond the Usual Suspects: Physiological Roles of the Arabidopsis Amidase Signature (AS) Superfamily Members in Plant Growth Processes and Stress Responses.

The diversification of land plants largely relies on their ability to cope with constant environmental fluctuations, which negatively impact their reproductive fitness and trigger adaptive responses to biotic and abiotic stresses. In this limiting landscape, cumulative research attention has centred on deepening the roles of major phytohormones, mostly auxins, together with brassinosteroids, jasmonates, and abscisic acid, despite the signaling networks orchestrating the crosstalk among them are so far only poorly understood. Accordingly, this review focuses on the Arabidopsis Amidase Signature (AS) superfamily members, with the aim of highlighting the hitherto relatively underappreciated functions of AMIDASE1 (AMI1) and FATTY ACID AMIDE HYDROLASE (FAAH), as comparable coordinators of the growth-defense trade-off, by balancing auxin and ABA homeostasis through the conversion of their likely bioactive substrates, indole-3-acetamide and N-acylethanolamine.

Endophytic Streptomyces hygroscopicus OsiSh-2-Mediated Balancing between Growth and Disease Resistance in Host Rice.

ABSTRACTPlants fine-tune the growth-defense trade-off to survive when facing pathogens. Meanwhile, plant-associated microbes, such as the endophytes inside plant tissues, can benefit plant growth and stress resilience. However, the mechanisms for the beneficial microbes to increase stress resistance with little yield penalty in host plants remain poorly understood. In the present study, we report that endophytic Streptomyces hygroscopicus OsiSh-2 can form a sophisticated interaction with host rice, maintaining cellular homeostasis under pathogen-infection stress, and optimize plant growth and disease resistance in rice. Four-year field trials consistently showed that OsiSh-2 could boost host resistance to rice blast pathogen Magnaporthe oryzae while still maintaining a high yield. The integration of the proteomic, physiological, and transcriptional profiling analysis revealed that OsiSh-2 induced rice defense priming and controlled the expression of energy-consuming defense-related proteins, thus increasing the defense capability with the minimized costs of plant immunity. Meanwhile, OsiSh-2 improved the chloroplast development and optimally maintained the expression of proteins related to plant growth under pathogen stress, thus promoting the crop yield. Our results provided a representative example of an endophyte-mediated modulation of disease resistance and fitness in the host plant. The multilayer effects of OsiSh-2 implicate a promising future of using endophytic actinobacteria for disease control and crop yield promotion.

European oak chemical diversity - from ecotypes to herbivore resistance.

Climate change is increasing insect pressure and forcing plants to adapt. Although chemotypic differentiation and phenotypic plasticity in spatially separated tree populations are known for decades, understanding their importance in herbivory resistance across forests remains challenging. We studied four oak forest stands in Germany using nontarget metabolomics, elemental analysis, and chemometrics and mapped the leaf metabolome of herbivore-resistant (T-) and herbivore-susceptible (S-) European oaks (Quercus robur) to Tortrix viridana, an oak pest that causes severe forest defoliation. Among the detected metabolites, we identified reliable metabolic biomarkers to distinguish S- and T-oak trees. Chemotypic differentiation resulted in metabolic shifts of primary and secondary leaf metabolism. Across forests, T-oaks allocate resources towards constitutive chemical defense enriched of polyphenolic compounds, e.g. the flavonoids kaempferol, kaempferol and quercetin glucosides, while S-oaks towards growth-promoting substances such as carbohydrates and amino-acid derivatives. This extensive work across natural forests shows that oaks' resistance and susceptibility to herbivory are linked to growth-defense trade-offs of leaf metabolism. The discovery of biomarkers and the developed predictive model pave the way to understand Quercus robur's susceptibility to herbivore attack and to support forest management, contributing to the preservation of oak forests in Europe.

Mechanisms of far-red light-mediated dampening of defense against Botrytis cinerea in tomato leaves.

Plants detect neighboring competitors through a decrease in the ratio between red and far-red light (R:FR). This decreased R:FR is perceived by phytochrome photoreceptors and triggers shade avoidance responses such as shoot elongation and upward leaf movement (hyponasty). In addition to promoting elongation growth, low R:FR perception enhances plant susceptibility to pathogens: the growth–defense tradeoff. Although increased susceptibility in low R:FR has been studied for over a decade, the associated timing of molecular events is still unknown. Here, we studied the chronology of FR-induced susceptibility events in tomato (Solanum lycopersicum) plants pre-exposed to either white light (WL) or WL supplemented with FR light (WL+FR) prior to inoculation with the necrotrophic fungus Botrytis cinerea (B.c.). We monitored the leaf transcriptional changes over a 30-h time course upon infection and followed up with functional studies to identify mechanisms. We found that FR-induced susceptibility in tomato is linked to a general dampening of B.c.-responsive gene expression, and a delay in both pathogen recognition and jasmonic acid-mediated defense gene expression. In addition, we found that the supplemental FR-induced ethylene emissions affected plant immune responses under the WL+FR condition. This study improves our understanding of the growth–immunity tradeoff, while simultaneously providing leads to improve tomato resistance against pathogens in dense cropping systems.