Insect Resistance: An Emerging Molecular Framework Linking Plant Age and JA Signaling

During developmental progression, also referred to as ontogeny, plants germinate into seedlings and pass through a vegetative juvenile stage, before reaching maturity at the onset of reproduction and senescing. Most of plants' physiological processes are profoundly reconfigured across ontogenetic stages, including those involved in defense against insect herbivores. For instance, increases in trait expression have been reported during development for anti-herbivore physical defenses like trichomes and spines, as well as for the constitutive accumulation of chemicals acting as insect deterrents (reviewed in Barton and Koricheva, 2010Barton K.E. Koricheva J. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis.Am. Nat. 2010; 175: 481-493Crossref PubMed Scopus (367) Google Scholar). In several plants, the intensity of induced responses to herbivore attack, as measured by the induced accumulation of hormones, transcripts, and metabolites, was shown to decay with the plant's age. This plasticity by which plants accumulate specific defensive traits only upon insect herbivory allows them to mitigate resource allocation costs to defense. Consequently, induced defenses are predicted to contribute more to a plant's survival against insect attacks during the initial stages of establishment of seedlings and juveniles. Several ecological theories invoking developmental, ecological, and evolutionary constraints have flourished to address the costs and benefits inherent to the deployment of ontogenetic defense patterns. The two most prominent ones, the Growth-Differentiation Balance (GDB) theory (Loomis, 1953Loomis W.E. Growth and differentiation—an introduction and summary.in: Loomis W.E. Growth and Differentiation in Plants. Iowa State University Press, Ames1953: 1-17Google Scholar) and the Optimal Defense (OD) theory (Mckey, 1974Mckey D. Adaptive patterns in alkaloid physiology.Am. Nat. 1974; 108: 305-320Crossref Google Scholar), propose hypotheses that respectively emphasize intrinsic (age-dependent trade-offs in the allocation of resources to defense) or extrinsic (age/tissue-dependent probability of herbivore attack conditioning the fitness benefit attributable to a defense) factors in the interaction of plants with insects. These two theories are non-mutually exclusive in the sense of the different levels of analyses that they address; metabolic resource allocation, fitness value, and risk of predation of a given tissue, are all expected to significantly vary during development. Nonetheless, testability of the functional perspectives provided by these theories is hampered by our fragmentary understanding of the molecular mechanisms connecting defense and development. Most herbivore resistance traits are regulated via the canonical jasmonic acid (JA) hormonal pathway. Herbivory-induced JA bursts frequently dampen during plant maturation (Diezel et al., 2011Diezel C. Allmann S. Baldwin I.T. Mechanisms of optimal defense patterns in Nicotiana attenuata: flowering attenuates herbivory-elicited ethylene and jasmonate signaling.J. Integr. Plant Biol. 2011; 53: 971-983Crossref PubMed Scopus (55) Google Scholar). These modulations are notably expected to result from the increasingly recognized interactions between the JA signaling and growth-related hormone sectors during defense responses (Meldau et al., 2012Meldau S. Erb M. Baldwin I.T. Defence on demand: mechanisms behind optimal defence patterns.Ann. Bot. 2012; 110: 1503-1514Crossref PubMed Scopus (123) Google Scholar). The conjugate (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile) is perceived by the Skp/Cullin/F-box SCFCOI E3 (COI1) ubiquitin ligase interacting with JA ZIM-domain (JAZ) proteins, which in normal conditions act as repressors of JA signaling (Pauwels and Goossens, 2011Pauwels L. Goossens A. The JAZ proteins: a crucial interface in the jasmonate signaling cascade.Plant Cell. 2011; 23: 3089-3100Crossref PubMed Scopus (429) Google Scholar). Upon insect herbivory or mechanical wounding, elevation of JA-Ile levels in plant cells triggers the formation of complexes between COI1 and the repertoire of JAZ proteins, resulting in tagging of JAZ proteins and degradation by the 26S proteasome. This process releases transcription factors, such as MYC2, to activate the expression of downstream defense genes. Important advances of the last decade in deciphering the molecular architecture of the JA signaling network have defined a regulatory playground in which to examine possible "molecular bridges" between JA signaling defense outputs and master regulators of age-dependent responses. One of these "molecular bridges" has recently been identified by Mao et al., 2017Mao Y.B. Liu Y.Q. Chen D.Y. Chen F.Y. Fang X. Hong G.J. Wang L.J. Wang J.W. Chen X.Y. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance.Nat. Commun. 2017; 8: 13925Crossref PubMed Scopus (126) Google Scholar as part of their study on modulations of JA signaling by the evolutionary conserved miRNA156(miR156)/SQUAMOSA-PROMOTER BINDING PROTEINs-LIKE (SPLs) regulatory module (Figure 1). The mi156/SPLs module functions as an aging cue regulating developmental processes such as flowering (Wang et al., 2009Wang J.W. Czech B. Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana.Cell. 2009; 138: 738-749Abstract Full Text Full Text PDF PubMed Scopus (1000) Google Scholar). High levels of miR156 during the juvenile stage decrease in an antiparallel fashion to increasing levels of sucrose as part of a plant's vegetative growth (Figure 1A). As a result of miR156 decay, levels of miR156-targeted SPLs increase, which notably accelerates reproductive phase change (Wu et al., 2009Wu G. Park M.Y. Conway S.R. Wang J.W. Weigel D. Poethig R.S. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis.Cell. 2009; 138: 750-759Abstract Full Text Full Text PDF PubMed Scopus (1139) Google Scholar). This regulatory loop ensures that developmental processes such as flowering take place when photosynthetic and metabolic capacities are adequate. The work by Mao et al., 2017Mao Y.B. Liu Y.Q. Chen D.Y. Chen F.Y. Fang X. Hong G.J. Wang L.J. Wang J.W. Chen X.Y. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance.Nat. Commun. 2017; 8: 13925Crossref PubMed Scopus (126) Google Scholar reveals a key interaction between this age-sensing module and JA signaling in Arabidopsis thaliana. Briefly, these authors provide experimental evidence that SPL9, a member of the SPL repertoire, negatively regulates herbivory-induced JA signaling (Figure 1B). Prolonged juvenile stage duration achieved by overexpression of miR156 or of an miR156-resistant SPL9 variant, attenuates the decay of herbivory-induced JA/JA-Ile levels normally observed during plant aging. The authors further demonstrate that SPL9 interacts with the N-terminal part of several JAZ proteins, particularly JAZ3. This interaction prevents the JA-Ile-triggered/COI1-mediated degradation of JAZ3, which consolidates its repressor activity over the JA-signaling-based induction of plant defenses. Glucosinolates are abundant secondary metabolites that contribute to the resistance of Brassicaceae species to insect herbivores. Although the amplitude of herbivory-induced JA/JA-Ile bursts dampens during vegetative aging of Arabidopsis plants, mature plants were found to be equipped with higher basal glucosinolate pools and had better resistance to generalist and specialist chewing insect herbivores than did younger plants (Mao et al., 2017Mao Y.B. Liu Y.Q. Chen D.Y. Chen F.Y. Fang X. Hong G.J. Wang L.J. Wang J.W. Chen X.Y. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance.Nat. Commun. 2017; 8: 13925Crossref PubMed Scopus (126) Google Scholar). This trend, apparently independent of the miR156/SPL9 module, highlights that the gradual increase of the glucosinolate pools might be one of major determinants of higher insect resistance detected in older plants (Figure 1C). Such uncoupling between ontogenetic trajectories of induced defense (here reflected by herbivory-induced levels of JA/JA-Ile and of their biosynthetic transcripts) and constitutive/basal defense strategies (here glucosinolate basal levels) has already been proposed in different ecological studies (Barton and Koricheva, 2010Barton K.E. Koricheva J. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis.Am. Nat. 2010; 175: 481-493Crossref PubMed Scopus (367) Google Scholar). Mao et al., 2017Mao Y.B. Liu Y.Q. Chen D.Y. Chen F.Y. Fang X. Hong G.J. Wang L.J. Wang J.W. Chen X.Y. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance.Nat. Commun. 2017; 8: 13925Crossref PubMed Scopus (126) Google Scholar propose that mobilization of glucosinolates from senescing to younger leaves, rather than upregulation of the glucosinolate biosynthetic machinery, protects younger leaves at mature stages of Arabidopsis plant development. This interpretation parallels predictions of the OD hypothesis concerning the optimal accumulation of defense compounds in tissues with higher fitness values for the plant and, along with discoveries in glucosinolate transport (Nour-Eldin et al., 2012Nour-Eldin H.H. Andersen T.G. Burow M. Madsen S.R. Jorgensen M.E. Olsen C.E. Dreyer I. Hedrich R. Geiger D. Halkier B.A. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds.Nature. 2012; 488: 531-534Crossref PubMed Scopus (328) Google Scholar), defines an interesting functional perspective to pursue. In summary, this novel crosstalk between JA signaling and the miR156/SPL9 aging module is an important piece in a bigger molecular puzzle controlling age-dependent modulations of plant defenses. Echoing the aforementioned ecological theories, open questions remain on how plants differentially prioritize induced versus constitutive defense at different developmental stages and on the ecological value of these management strategies in real-world conditions. The research work of E.G. and M.S. is supported by the University of Heidelberg.