Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis

Bekaert, Michaël; Edger, Patrick P.; Hudson, Corey; Pires, J. Chris; Conant, Gavin C.

doi:10.1111/j.1469-8137.2012.04302.x

Cited by 166 publications

(132 citation statements)

References 81 publications

(126 reference statements)

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“…spines and trichomes) and specific chemical compounds. Constitutive defense mechanisms provide immediate protection against herbivore attacks, although they represent an energy investment by the plant regardless of whether herbivory occurs or not (Mauricio, 1998;Bekaert et al, 2012). By contrast, inducible defense mechanisms do not require an up-front energy cost, although such mechanisms may not be as immediate as constitutive ones when herbivore feeding occurs (Windram et al, 2012).…”

mentioning

confidence: 99%

Reexamination of Chlorophyllase Function Implies Its Involvement in Defense against Chewing Herbivores

Makita

Schelbert

et al. 2015

Plant Physiol.

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Chlorophyllase (CLH) is a common plant enzyme that catalyzes the hydrolysis of chlorophyll to form chlorophyllide, a more hydrophilic derivative. For more than a century, the biological role of CLH has been controversial, although this enzyme has been often considered to catalyze chlorophyll catabolism during stress-induced chlorophyll breakdown. In this study, we found that the absence of CLH does not affect chlorophyll breakdown in intact leaf tissue in the absence or the presence of methyljasmonate, which is known to enhance stress-induced chlorophyll breakdown. Fractionation of cellular membranes shows that Arabidopsis (Arabidopsis thaliana) CLH is located in the endoplasmic reticulum and the tonoplast of intact plant cells. These results indicate that CLH is not involved in endogenous chlorophyll catabolism. Instead, we found that CLH promotes chlorophyllide formation upon disruption of leaf cells, or when it is artificially mistargeted to the chloroplast. These results indicate that CLH is responsible for chlorophyllide formation after the collapse of cells, which led us to hypothesize that chlorophyllide formation might be a process of defense against chewing herbivores. We found that Arabidopsis leaves with genetically enhanced CLH activity exhibit toxicity when fed to Spodoptera litura larvae, an insect herbivore. In addition, purified chlorophyllide partially suppresses the growth of the larvae. Taken together, these results support the presence of a unique binary defense system against insect herbivores involving chlorophyll and CLH. Potential mechanisms of chlorophyllide action for defense are discussed.

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confidence: 99%

Reexamination of Chlorophyllase Function Implies Its Involvement in Defense against Chewing Herbivores

Makita

Schelbert

et al. 2015

Plant Physiol.

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“…Combined with the guiltby-association principle (Bino et al, 2004;Saito et al, 2008), omics analyses allow the prediction of unknown gene and metabolite functions. For instance, the systematic metabolomics approach has helped to determine the biosynthetic regulation of glucosinolates by MYB transcription factors (Hirai et al, 2007;Sønderby et al, 2007) and to model the costs of glucosinolate biosynthesis in terms of primary metabolism (Bekaert et al, 2012). This data-driven (top-down) strategy can guide the development of new hypotheses about regulatory and metabolic pathways, which may subsequently predict the emergence of certain phenotypes (Fukushima et al, 2009;Saito and Matsuda, 2010).…”

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confidence: 99%

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

et al. 2016

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Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O 3 ), a global anthropogenic pollutant, directly affects living organisms and ecosystems, including plant-herbivore interactions. In this study, we investigate the stress responses of Brassica nigra (wild black mustard) exposed consecutively to O 3 and the specialist herbivore Pieris brassicae. Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O 3 and herbivory responses. O 3 stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O 3 to herbivory induced characteristic plant defense responses, including a decrease in central metabolism, induction of the jasmonic acid/ethylene pathways, and emission of volatiles. Omics network and pathway analyses predicted a link between glycerol and central energy metabolism that influences the osmotic stress response and stomatal closure. Further physiological measurements confirmed that while O 3 stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O 3 , resulting in a phenotype similar to that observed after herbivory alone. This study clarifies the consequences of multiple stress interactions on a plant metabolic system and also illustrates how omics data can be integrated to generate new hypotheses in ecology and plant physiology.

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“…Allocation of glucosinolates could be one of the tolerance strategies to cope with stressful conditions with relative low energy cost. A direct allocation of glucosinolates production in Arabidopsis with an increase in photosynthetic energy has been reported by Bekaert et al [109]. These all findings indicated that salt-induced increases in glucosinolates content may be involved in the salt stress response of plants but the effects of salinity on glucosinolates biosynthesis and metabolism need further attention at molecular and cellular levels.…”

Section: Glucosinolatesmentioning

confidence: 77%

Salinity Tolerance in Plants: Revisiting the Role of Sulfur Metabolites

Khan¹,

Khan²,

Asgher³

et al. 2014

J Plant Biochem Physiol

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IntroductionSalinity is a major abiotic stress which adversely affects plant processes at physiological, biochemical and molecular level and reduces plant productivity [1,2]. The fertility status of soil is deteriorating due to increasing salinity levels and has been a subject of concern to agricultural scientists for sustainable developments of crops [3]. It is expected to result in the loss of up to 50% fertile land by the middle of the 21 st century [4]. The loss in plant productivity due to salinity has been associated to imbalance in ionic and nutrients status of plants [5,6], overproduction of Reactive Oxygen Species (ROS) and redox state of cell. The consequence of ROS overproduction in chloroplast, mitochondria and peroxisomes is damage to lipids, proteins, nucleic acids and integrity of cell membrane properties [7,8]. Among various mechanisms adopted by plants to cope with the increasing salinityinduced oxidative stress, maintaining redox state of cell through increased sulfur (S) metabolism and production of S-containing compounds are of paramount importance. It is, therefore, necessary to consolidate our understanding on the S metabolism for improving salinity tolerance in plants. As S is an essential element for all living organisms and occupies fourth place in importance after nitrogen (N), phosphorus (P) and potassium (K) in agricultural system, it could emerge as an element necessarily required for sustainability of crop plants under abiotic stress. Khan et al. [9] and Nocito [10] have shown that S is necessary for abiotic stress tolerance of plants being an integral part of major metabolic compounds, such as amino acids (methionine; Met and cysteine; Cys), antioxidant (GSH), proteins, and sulfolipids. In addition, S is also a component of iron-S-clusters, polysaccharides and lipids and a broad variety of biomolecules including vitamins (biotin and thiamine), cofactors (CoA and S-adenosyl-Met), peptides (GSH and phytochelatins) and secondary products (allyl-cysteine sulphoxides and glucosinolates).It is expected that modulation of S metabolism in plants would help in alleviating adverse effects of salinity as its metabolites control wide range of plant processes. The production of S-containing compounds through S metabolism is linked to antioxidant system in plants under salinity stress (Figure 1). Studies have revealed various aspects of salinity tolerance mechanisms [5,[11][12][13], but a consolidated approach on salinity AbstractSalinity is becoming a major threat to plant productivity loss in agricultural system. Plants respond to saline environment by modulating the inherent mechanisms to adjust to the changing environment. The understanding of the mechanisms that plants operate under saline environment is essential beginning in efforts to reduce the adverse effects of salinity stress. The agricultural system is tightly linked with the fertilizer input and thus the judicious application of fertilizers is expected to lead positive effects in reversing the salinity effects. Sulfur is a macron...

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Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis

Cited by 166 publications

References 81 publications

Reexamination of Chlorophyllase Function Implies Its Involvement in Defense against Chewing Herbivores

Reexamination of Chlorophyllase Function Implies Its Involvement in Defense against Chewing Herbivores

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

Salinity Tolerance in Plants: Revisiting the Role of Sulfur Metabolites

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