Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs

Denancé, Nicolás; Sánchez‐Vallet, Andrea; Goffner, Deborah; Molina, Antonio

doi:10.3389/fpls.2013.00155

Cited by 550 publications

(464 citation statements)

References 160 publications

(214 reference statements)

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“…5B and Dataset S1, Table S4), suggesting that the small plant line has higher basal expression levels of the defense response genes. These observations support the suggestion that there is a negative relationship between vegetative growth and defense activation (26,27), with the down-regulated defense-related gene activities associated with greater growth of the hybrids and hybrid mimic plants.…”

Section: Genes and Metabolic Pathways Important In The F1 Hybrid Phensupporting

confidence: 85%

“…The common property of genes involved in a number of the defense response pathways was their down-regulation relative to midparental values. This property fits with proposals that there is antagonism between defense response pathways and growth pathways (26,27). This counterbalancing of energy-consuming gene activities and growth is emphasized by the finding that, in small plant phenotypes, there are gene activity profiles opposite to those of the large hybrid mimics, where a number of defense response genes are up-regulated and the vegetative size of the plants is reduced.…”

Section: Genes and Metabolic Pathways Important In The F1 Hybrid Phensupporting

confidence: 84%

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Hybrid mimics and hybrid vigor in Arabidopsis

Wang

Greaves

Groszmann

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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F1 hybrids can outperform their parents in yield and vegetative biomass, features of hybrid vigor that form the basis of the hybrid seed industry. The yield advantage of the F1 is lost in the F2 and subsequent generations. In Arabidopsis, from F2 plants that have a F1-like phenotype, we have by recurrent selection produced pure breeding F5/F6 lines, hybrid mimics, in which the characteristics of the F1 hybrid are stabilized. These hybrid mimic lines, like the F1 hybrid, have larger leaves than the parent plant, and the leaves have increased photosynthetic cell numbers, and in some lines, increased size of cells, suggesting an increased supply of photosynthate. A comparison of the differentially expressed genes in the F1 hybrid with those of eight hybrid mimic lines identified metabolic pathways altered in both; these pathways include down-regulation of defense response pathways and altered abiotic response pathways. F6 hybrid mimic lines are mostly homozygous at each locus in the genome and yet retain the large F1-like phenotype. Many alleles in the F6 plants, when they are homozygous, have expression levels different to the level in the parent. We consider this altered expression to be a consequence of transregulation of genes from one parent by genes from the other parent. Transregulation could also arise from epigenetic modifications in the F1. The pure breeding hybrid mimics have been valuable in probing the mechanisms of hybrid vigor and may also prove to be useful hybrid vigor equivalents in agriculture.I n Arabidopsis some ecotypes with similar genome sequences produce F1 hybrids with large increases in vegetative and reproductive yields (1, 2). These results appear to be at variance with the generalization that the larger the genetic distance between parents, the greater the hybrid vigor (3); however, the Arabidopsis ecotypes have different epigenomes that may be important for hybrid vigor (4). In hybrids between C24 and Ler, we found altered levels in two epigenetic systems: 24nt siRNAs and DNA methylation (4, 5). These epigenetic changes appear common among hybrid systems with similar observations being made in maize and rice hybrids (6). The epigenetic changes can correlate with changes in gene expression and contribute to the unique gene expression profile of the F1 hybrid (7). Not all crosses result in hybrid vigor (heterosis); some result in decreased vigor and yield referred to as "hybrid weakness" (8).Heterotic F1 hybrids are featured in agricultural and horticultural crops, and in all species, the yield gains are restricted to the F1 generation. The F2 and subsequent selfed generations are discarded because of reduced yields and heterogeneity of morphological and developmental traits. A hybrid crop system requires an efficient method of F1 hybrid seed production dependent on male sterility in the female parent and synchronous flowering of the male and female parents.QTL analysis in maize and rice has confirmed that hundreds of genome segments contribute to the heterotic phenotype, but the main m...

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Section: Genes and Metabolic Pathways Important In The F1 Hybrid Phensupporting

confidence: 85%

Section: Genes and Metabolic Pathways Important In The F1 Hybrid Phensupporting

confidence: 84%

Hybrid mimics and hybrid vigor in Arabidopsis

Wang

Greaves

Groszmann

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…ABA is a major regulator of abiotic stress responses caused by drought, salt, cold and wounding (Christmann et al ., 2006; Raghavendra et al ., 2010), and also plays a prominent role in plant resistance to biotic stresses such as pathogen attack (Ton et al ., 2009; Denance et al ., 2013) and herbivorous insects (Bodenhausen and Reymond, 2007; Verhage et al ., 2011; Pineda et al ., 2012; Lazebnik et al ., 2014). In our study, ABA content was increased in the Arabidopsis leaves when it was inoculated with T. gamsii F18.…”

Section: Discussionmentioning

confidence: 99%

Trichoderma gamsii affected herbivore feeding behaviour on Arabidopsis thaliana by modifying the leaf metabolome and phytohormones

Zhou

Huang

Guo

et al. 2018

Microbial Biotechnology

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SummaryPlants can re‐programme their transcriptome, proteome and metabolome to deal with environmental and biotic stress. It has been shown that the rhizosphere microbiome has influence on the plant metabolome and on herbivore behaviour. In the present study, Trichoderma gamsii was isolated from Arabidopsis thaliana rhizosphere soil. The inoculation of roots of Arabidopsis thaliana with T. gamsii significantly inhibited the feeding behaviour of Trichoplusia ni and affected the metabolome as well as the content of phytohormones in Arabidopsis leaves. T. gamsii‐treated plant leaves had higher levels of amino acids and lower concentrations of sugars. In addition, T. gamsii‐treated plant leaves had more abscisic acid (ABA) and lower levels of salicylic acid (SA) and indole‐3‐acetic acid (IAA) in comparison with the untreated plants. Furthermore, the inoculation with T. gamsii on different signalling mutants showed that the induction of defences were SA‐dependent. These findings indicate that T. gamsii has potential as a new type of biocontrol agent to promote plant repellence to insect attacks.

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“…The patterns of altered defense-related gene expression imply that the hybrids have a decreased basal defense response, this being more pronounced in the C24/Ler and C24/Col hybrids. Given the antagonistic relationship between plant immunity and plant growth (7,8), the lower level of defense-related metabolism could be significant for generating the greater growth of the hybrids.…”

Section: Gene Regulatory Network Involved In Defense and Stress Respmentioning

confidence: 99%

“…We found that all of the hybrids have transcription profiles implying increased stress tolerance and suppression of defense-related pathways as major altered processes, although the exact patterns of change differ between the hybrids. Given the competition between plant immunity and plant growth for resource allocation (7,8), the reduction in basal defense levels could be important for generating heterosis. Substantial changes in the auxin [indole-3-acetic acid (IAA)]-and salicylic acid…”

mentioning

confidence: 99%

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

Groszmann

González-Bayón

Lyons

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

124

115

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Plant hybrids are extensively used in agriculture to deliver increases in yields, yet the molecular basis of their superior performance (heterosis) is not well understood. Our transcriptome analysis of a number of Arabidopsis F1 hybrids identified changes to defense and stress response gene expression consistent with a reduction in basal defense levels. Given the reported antagonism between plant immunity and growth, we suggest that these altered patterns of expression contribute to the greater growth of the hybrids. The altered patterns of expression in the hybrids indicate decreases to the salicylic acid (SA) biosynthesis pathway and increases in the auxin [indole-3-acetic acid (IAA)] biosynthesis pathway. SA and IAA are hormones known to control stress and defense responses as well as plant growth. We found that IAA-targeted gene activity is frequently increased in hybrids, correlating with a common heterotic phenotype of greater leaf cell numbers. Reduced SA concentration and target gene responses occur in the larger hybrids and promote increased leaf cell size. We demonstrated the importance of SA action to the hybrid phenotype by manipulating endogenous SA concentrations. Increasing SA diminished heterosis in SA-reduced hybrids, whereas decreasing SA promoted growth in some hybrids and phenocopied aspects of hybrid vigor in parental lines. Pseudomonas syringae infection of hybrids demonstrated that the reductions in basal defense gene activity in these hybrids does not necessarily compromise their ability to mount a defense response comparable to the parents.

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Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs

Cited by 550 publications

References 160 publications

Hybrid mimics and hybrid vigor in Arabidopsis

Hybrid mimics and hybrid vigor in Arabidopsis

Trichoderma gamsii affected herbivore feeding behaviour on Arabidopsis thaliana by modifying the leaf metabolome and phytohormones

Hormone-regulated defense and stress response networks contribute to heterosis inArabidopsisF1 hybrids

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