Magnitude and Timing of Leaf Damage Affect Seed Production in a Natural Population of Arabidopsis thaliana (Brassicaceae)

Akiyama, Reiko; Ågren, Jon

doi:10.1371/journal.pone.0030015

Cited by 28 publications

(25 citation statements)

References 51 publications

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“…The effects of plant phenology traits on tolerance largely mirror the results of studies exploring the impact of the timing of damage on tolerance, which again have primarily been within‐species, and on herbaceous monocarpic species (Maschinski and Whitham , Trumble et al. , Lowenberg , Del‐Val and Crawley , Akiyama and Ågren , Hoque and Avila‐Sakar ). Typically, compensation or overcompensation for damage has been documented in short‐lived monocarpic plants experiencing browse that removes apical dominance and that (over)compensate through increased inflorescence production from branching, e.g., Ipomopsis aggregata (Paige and Whitham ), Gentianella campestris (Juenger et al.…”

Section: Introductionmentioning

confidence: 82%

Macroevolutionary constraints to tolerance: trade‐offs with drought tolerance and phenology, but not resistance

Pearse

Aguilar

Schroder

et al. 2017

Ecology

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Plant tolerance of herbivory, i.e., the ability to recover after damage, is an important component of how plants cope with herbivores. Tolerance has long been hypothesized to be constrained evolutionarily by plant resistance to herbivores, traits that allow plants to cope with stressful growing conditions, and traits that influence the timing of damage in relation to reproduction. Variation in tolerance and resistance can be caused by differences in the identity of the plant (e.g., genotype, species, clade) and by the context of the herbivore threat (e.g., identity of the herbivore, type of damage it causes, abiotic conditions in which the plant is growing). To date, the vast majority of studies have explored trade-offs with tolerance within species. Here, we test hypotheses of constraints on tolerance using comparative approaches in a clade of mustards, emphasizing the variety of contexts in which damage is realistically tolerated. We estimated tolerance to leaf damage, tolerance to apical clipping at the bolting stage - simulating browsing -, and resistance to a specialist and generalist lepidopteran herbivore for a group of native mustards, grown in field soils unique to each population and in a common potting soil. Resistance to herbivores was soil dependent, while surprisingly, tolerance was not. Phylogenetic signal in resistance to specialist and generalist lepidopteran herbivores was present, but only when plants were grown in field soils. Tolerance had low phylogenetic signal. Tolerance to leaf damage was unrelated to tolerance to simulated browse. We found no evidence for a resistance-tolerance trade-off, and some evidence for a soil-dependent positive correlation between tolerance and resistance to both herbivores. Drought-tolerant species had poorer ability to tolerate browse damage, and earlier flowering species tended to be less tolerant to leaf damage. Our results suggest that tolerance trades off with traits that allow mostly annual, monocarpic Streptanthus (s.l.) to persist in drought-prone conditions but is largely unrelated to resistance to herbivores. Our study highlights a need for a new framework for tolerance to herbivory that explicitly acknowledges that the relationship among tolerance, resistance, and traits that ameliorate abiotic stress.

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Section: Introductionmentioning

confidence: 82%

Macroevolutionary constraints to tolerance: trade‐offs with drought tolerance and phenology, but not resistance

Pearse

Aguilar

Schroder

et al. 2017

Ecology

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“…Ida et al also suggested that although defoliation in Oxytropis sericea reduced photosynthesis and nectar production, it did not alter photosynthate allocation or fruit or seed production [38]. However, Akiyama and Ågren demonstrated that defoliation in Arabidopsis thaliana reduced seed production, and this reduction correlated negatively with the removed leaf area [39]. The above contradictory results suggest that defoliation is a complex process, which includes defoliation timing, intensity, and species tolerance, and may lead to different responses.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome Analysis Reveals Common and Distinct Mechanisms for Sheepgrass (Leymus chinensis) Responses to Defoliation Compared to Mechanical Wounding

et al. 2014

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BackgroundHerbivore grazing is a multiple-component process that includes wounding, defoliation, and saliva deposition. Despite the extensive published research on mechanical wounding and defoliation, no analysis to identify the genes that specify defoliation and mechanical wounding has been performed. Moreover, the influence of the expression of these genes on plant regrowth after defoliation remains poorly understood.ResultsSeven cDNA libraries for RNA samples collected from stubble tissues that had been mechanically wounded or defoliated at 2, 6 and 24 h along with the control were sequenced using the Illumina/Solexa platform. A comparative transcriptomic analysis of the sequencing data was conducted. In total, 1,836 and 3,238 genes were detected with significant differential expression levels after wounding and defoliation, respectively, during one day. GO, KOG and pathway-based enrichment analyses were performed to determine and further understand the biological functions of those differentially expressed genes (DEGs). The results demonstrated that both wounding and defoliation activated the systemic synthesis of jasmonate (JA). However, defoliation specifically reduced the expression levels of ribosomal protein genes, cell division or cell expansion-related genes, and lignin biosynthesis genes and may have negatively affected plant growth. Further analysis revealed that the regrowth of elongating leaves was significantly retarded after defoliation at 6 h through the following 7 days of measurement, suggesting that the gene expression pattern and phenotype are consistent. Fifteen genes were selected, and their expression levels were confirmed by quantitative RT-PCR (qRT-PCR). Thirteen of them exhibited expression patterns consistent with the digital gene expression (DGE) data.ConclusionsThese sequencing datasets allowed us to elucidate the common and distinct mechanisms of plant responses to defoliation and wounding. Additionally, the distinct DEGs represent a valuable resource for novel gene discovery that may improve plant resistance to defoliation from various processes.

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“…Also, changes in seed composition due to defoliation appear to be a rather common phenomenon since, similarly to grain amaranth, loss of leaf tissue has been observed to lead to changes in composition, size or yield in many plant species [73], [74].…”

Section: Discussionmentioning

confidence: 99%

Grain Amaranths Are Defoliation Tolerant Crop Species Capable of Utilizing Stem and Root Carbohydrate Reserves to Sustain Vegetative and Reproductive Growth after Leaf Loss

et al. 2013

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Tolerance to defoliation can be defined as the degree to which productivity is affected by photosynthetic area reduction. This trait was studied in grain amaranth (Amaranthus cruentus and A. hypochondriacus), which are considered to be a highly defoliation-tolerant species. The physiological and biochemical responses to increasing levels of mechanical leaf removal up to total defoliation were quantified. Tolerance appeared to be dependent on various factors: ( i) amount of lost tissue; (ii) mechanics of leaf tissue removal; (iii) environment, and (iv) species tested. Thus, grain amaranth was found to be a highly tolerant species under green-house conditions when leaf tissue loss was performed by gradual perforation. However, tolerance was compromised under similar conditions when defoliation was done by gradual cutting of the leaf. Also tolerance in completely defoliated plants tended to decrease under field conditions, where differences between A. cruentus and A. hypochondriacus were observed. All non-structural carbohydrate (NSC) levels were reduced in stems and roots of totally defoliated amaranths one day after treatment. Such depletion probably provided the carbon (C) resources needed to sustain the early recovery process in the absence of photosynthetic capacity. This was corroborated by shading of intact plants, which produced the same rapid and drastic reduction of NSC levels in these tissues. These results emphasize the role of stored NSCs, particularly starch, in buffering the impact of severe defoliation in amaranth. The fall in sucrose synthase and cell wall invertase activity observed in stems and roots soon after defoliation was consistent with their predicted shift from sink to source tissues. It is concluded that mobilization of C stores in stems and roots, is a physiologically important trait underlying tolerance to defoliation in grain amaranth.

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Magnitude and Timing of Leaf Damage Affect Seed Production in a Natural Population of Arabidopsis thaliana (Brassicaceae)

Cited by 28 publications

References 51 publications

Macroevolutionary constraints to tolerance: trade‐offs with drought tolerance and phenology, but not resistance

Macroevolutionary constraints to tolerance: trade‐offs with drought tolerance and phenology, but not resistance

Transcriptome Analysis Reveals Common and Distinct Mechanisms for Sheepgrass (Leymus chinensis) Responses to Defoliation Compared to Mechanical Wounding

Grain Amaranths Are Defoliation Tolerant Crop Species Capable of Utilizing Stem and Root Carbohydrate Reserves to Sustain Vegetative and Reproductive Growth after Leaf Loss

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