Within‐plant relationships among wounding, jasmonic acid, and nicotine implications for defence in Nicotiana sylvestris

Abstract

SVMM.^HYIn Nicotiana .n'hestris Spegazzini and Comes {Solanaceae), we examined the relationships among wounding, endogenous leaf jasmonic acid (JA) pools, and whole-plant (\VP) nicotine accumulation ovet a range of woundmg intensities and spatial distributions, in order to explore optimal defence (OD) theory-predictions. We quantitatively wounded one or four leaves and then quantified: (1) JA in damaged and undamaged leaves 90 min after wounding; (2) WP nicotine concentration after 5 d (the times when JA and nicotine attain the largest wound-induced concentrations). We find: (1) statistically significant, positive relationships on a !eaf-by-leaf basis among tbe number of leaf punctures, endogenous leaf JA, and WP nicotine accumulation; (2) tbat young, undamaged leaves have a bigber concentration of JA tban do older, undamaged leaves, and produce a greater amount of JA per puncture tban older leaves, but tbat all leaves bave tbe same JA content (ng JA per leaf); and (3) that a damaged leaf produces less JA when other leaves in tbe canopy are wounded than when it is the only wounded leaf in tbe canopy, but tbat when it is tbe only wounded ieaf, tbe pbylotactically adjacent, undamaged leaves do not mcrease their JA concentrations. Tbe observation tbat younger leaves produce more JA per puncture tban do older leaves is consistent with OD theory predictions. The observation that a small amount of damage localized to a single leaf is as effective as a larger amount of damage dispersed across the canopy in increasing leaf JA and WP nicotine accumulation shows the plant's ability to differentiate between dispersed and localized damage. Because the quantity of JA in a wounded leaf 90 min after wounding is a reliable indicator of the WP nicotine response to wounding, this trait provides insight into how plants integrate information about environmental insults and tailor tbeir defence responses.

Jasmonate-induced responses are costly but benefit plants under attack in native populations

“…Each population contained more than 1,000 plants growing among the charred stumps of Juniperus spp. When the pairs were labeled and treated (April 19-23 and May 13, 1996 for the populations in 2-year-old burns and May [22][23][24][25][26][27][28]1996 for the populations in 1-year-old burns), plants in a pair grew within 40-120 cm of each other and were undamaged and of the same rosette diameter (Ϯ0.5 cm). At the time of treatment, all plants were in the rosette stage of growth with diameters that ranged from 5 to 22 cm.…”

“…Jasmonic acid (JA), a ubiquitous wound hormone known to increase the synthesis of diverse defense-related metabolites (1,20,21), is strongly implicated as a long-distance endogenous wound signal, activating nicotine synthesis in the roots after leaf wounding (22,23). Leaf wounding dramatically increases endogenous JA levels (5-500 ng per plant) within 90 min after wounding in proportion to the amount of wounding (23)(24)(25), and these endogenous levels of JA are strongly correlated with the whole-plant nicotine response 5 days later (23,24). Inhibition of the wound-induced JA response in the leaves with lypoxygenase and cyclooxidase inhibitors inhibits the nicotine response (23,26); the addition of JA and its methyl ester, MeJA, to the roots of both hydroponically and soil-grown plants increases de novo nicotine synthesis and whole-plant nicotine accumulations just as leaf damage does (12).…”

“…All pairs of plants selected for analysis were unattacked (with less than 5% leaf area lost to herbivores at the time of sampling) except those from population IIB, all of whose pairs had been attacked, so the least-attacked pairs were selected for analysis. Leaves were air-dried with a battery-powered fruit drier or in a convection oven at temperatures below 90°C, sealed in plastic bags, and shipped to the laboratory for nicotine analysis by HPLC with an external standard quantification technique (15,24). Nicotine loss during drying and shipping was quantified by including approximately 0.5 g of freeze-dried N. attenuata leaves of known nicotine concentration with each batch of samples.…”

APETALA2/ETHYLENE RESPONSE FACTOR and basic helix–loop–helix tobacco transcription factors cooperatively mediate jasmonate‐elicited nicotine biosynthesis

“…Changes in JA concentrations control the biosynthesis of nicotine and other pyridine alkaloids in tobacco (Nicotiana tabacum) together with other development-and stress-related signals (Baldwin et al, 1996;Ohnmeiss et al, 1997). The expression of structural genes involved in nicotine biosynthesis is stimulated by methyl jasmonate (MeJA) in cultured cells or hairy roots of Nicotiana species (Imanishi et al, 1998;Goossens et al, 2003;Cane et al, 2005).…”

Molecular, Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds

“…In addition, elicitors of plant defenses, including various fatty acidamino acid conjugates, have been isolated from caterpillar regurgitant (Alborn et al, 1997;Pohnert et al, 1999;Halitschke et al, 2001). Mechanical wounding and elicitors in the caterpillar's oral secretions activate the jasmonate pathway, leading to the production of jasmonic acid (JA) and induction of defenses against many challengers (Farmer and Ryan, 1992;Karban and Baldwin, 1997;McCloud and Baldwin, 1997;Ohnmeiss et al, 1997;Moura and Ryan, 2001).…”