The dynamics of recovery and growth: how defoliation affects stored resources

Growth rate varies widely among species and the trade-off between growth rate and storage or maintenance traits is a principal axis of variation between species. Many plant species have substantial root stores, but very little is known about how growth rate modifies responses of these stores to defoliation and other stresses. Species with different growth rates are predicted to respond in distinct ways, because of variation in the pre-defoliation allocation to storage. Here, we quantified the dynamics of stored carbohydrates in seven species with varying growth rate, following defoliation in a pot experiment. For faster growing species, there was significant reduction in carbohydrate concentration following defoliation, followed by relatively fast recovery, whereas for slower growing species, carbohydrate concentration levels remained relatively invariant across treatments. Results for total carbohydrates mirrored those for concentration, but were not as significant. Our findings were consistent with the idea that faster growing species respond more rapidly than slower growers to defoliation, through changes in carbohydrate pool concentrations. Growth rate as an indicator of life-history and ecological strategy may therefore be key to understanding post-defoliation recovery and storage strategies.     

Jasmonate‐mediated stomatal closure under elevated CO2 revealed by time‐resolved metabolomics

Foliar stomatal movements are critical for regulating plant water loss and gas exchange. Elevated carbon dioxide (CO₂) levels are known to induce stomatal closure. However, the current knowledge on CO₂ signal transduction in stomatal guard cells is limited. Here we report metabolomic responses of Brassica napus guard cells to elevated CO₂ using three hyphenated metabolomics platforms: gas chromatography‐mass spectrometry (MS); liquid chromatography (LC)‐multiple reaction monitoring‐MS; and ultra‐high‐performance LC‐quadrupole time‐of‐flight‐MS. A total of 358 metabolites from guard cells were quantified in a time‐course response to elevated CO₂ level. Most metabolites increased under elevated CO₂, showing the most significant differences at 10 min. In addition, reactive oxygen species production increased and stomatal aperture decreased with time. Major alterations in flavonoid, organic acid, sugar, fatty acid, phenylpropanoid and amino acid metabolic pathways indicated changes in both primary and specialized metabolic pathways in guard cells. Most interestingly, the jasmonic acid (JA) biosynthesis pathway was significantly altered in the course of elevated CO₂ treatment. Together with results obtained from JA biosynthesis and signaling mutants as well as CO₂ signaling mutants, we discovered that CO₂‐induced stomatal closure is mediated by JA signaling.     

去叶对青杨雌雄植株生长和非结构性碳水化合物的影响

近年来,森林食叶害虫在全世界呈爆发趋势.树木的非结构性碳水化合物(NSC)如何响应叶片损失对其生长和生存至关重要.雌雄异株植物在维持森林生态系统稳定性方面扮演着重要角色.然而,目前对该类植物性别之间如何响应去叶的研究还比较少.本文以我国重要的经济和生态恢复树种青杨(Populus cathayana)为研究材料,比较了...     

The maize lipoxygenase,ZmLOX10, mediates green leaf volatile,jasmonate and herbivore‐induced plant volatile production for defense against insect attack

Fatty acid derivatives are of central importance for plant immunity against insect herbivores; however, major regulatory genes and the signals that modulate these defense metabolites are vastly understudied, especially in important agro‐economic monocot species. Here we show that products and signals derived from a single Zea mays (maize) lipoxygenase (LOX), ZmLOX10, are critical for both direct and indirect defenses to herbivory. We provide genetic evidence that two 13‐LOXs, ZmLOX10 and ZmLOX8, specialize in providing substrate for the green leaf volatile (GLV) and jasmonate (JA) biosynthesis pathways, respectively. Supporting the specialization of these LOX isoforms, LOX8 and LOX10 are localized to two distinct cellular compartments, indicating that the JA and GLV biosynthesis pathways are physically separated in maize. Reduced expression of JA biosynthesis genes and diminished levels of JA in lox10 mutants indicate that LOX10‐derived signaling is required for LOX8‐mediated JA. The possible role of GLVs in JA signaling is supported by their ability to partially restore wound‐induced JA levels in lox10 mutants. The impaired ability of lox10 mutants to produce GLVs and JA led to dramatic reductions in herbivore‐induced plant volatiles (HIPVs) and attractiveness to parasitoid wasps. Because LOX10 is under circadian rhythm regulation, this study provides a mechanistic link to the diurnal regulation of GLVs and HIPVs. GLV‐, JA‐ and HIPV‐deficient lox10 mutants display compromised resistance to insect feeding, both under laboratory and field conditions, which is strong evidence that LOX10‐dependent metabolites confer immunity against insect attack. Hence, this comprehensive gene to agro‐ecosystem study reveals the broad implications of a single LOX isoform in herbivore defense.     

Overall grazing tolerance index (overall GTI) is not an ideal predictor for describing a single‐species tolerance to grazing

Plants' pattern of compensatory growth is often used to intuitively estimate their grazing tolerance. However, this tolerance is sometimes measured by the overall grazing tolerance index (overall GTI), which assumes that tolerance is a multivariate linear function of various underlying mechanisms. Because the interaction among mechanisms is not independent, the grazing tolerance expression based on overall GTI may be inconsistent with that based on compensatory growth. Through a manipulative field experiment from 2007 to 2012, we measured the responses of 12 traits of Elymus nutans to clipping under different resource availabilities in an alpine meadow and explored the compensatory aboveground biomass and the overall GTI to assess the possible differences between the two expressions of tolerance. Our results showed that these two expressions of tolerance were completely opposite. The expression based on overall GTI was over‐compensatory and did not vary with clipping and resource availability, while the expression based on compensatory aboveground biomass was under‐compensatory and altered to over‐compensation after fertilization. The over‐expression of highly variable traits with extremely high negative mean GTI to defoliation damage, the influence of random errors contained in traits considered, and the doubling weight of functional redundant traits greatly inflated the overall GTI, which leads to the inconsistency of the two tolerance expressions. This inconsistency is also associated with the different determining mechanisms of the two tolerance expressions. Our data suggest that plants' grazing tolerance is not a multivariate linear function of traits or mechanisms that determine grazing tolerance; the overall GTI is only a measure of traits' variability to defoliation damage. Our findings highlight that the tolerance of E. nutans mainly depends on the response of traits with lower variability to defoliation, and the overall GTI is not an ideal predictor for describing a single‐species tolerance to grazing.     

Jasmonoyl‐l‐isoleucine hydrolase 1 (JIH1) regulates jasmonoyl‐l‐isoleucine levels and attenuates plant defenses against herbivores

For most plant hormones, biological activity is suppressed by reversible conjugation to sugars, amino acids and other small molecules. In contrast, the conjugation of jasmonic acid (JA) to isoleucine (Ile) is known to enhance the activity of JA. Whereas hydroxylation and carboxylation of JA‐Ile permanently inactivates JA‐Ile‐mediated signaling in plants, the alternative deactivation pathway of JA‐Ile by its direct hydrolysis to JA remains unstudied. We show that Nicotiana attenuata jasmonoyl‐l ‐isoleucine hydrolase 1 (JIH1), a close homologue of previously characterized indoleacetic acid alanine resistant 3 (IAR3) gene in Arabidopsis, hydrolyzes both JA‐Ile and IAA‐Ala in vitro. When the herbivory‐inducible NaJIH1 gene was silenced by RNA interference, JA‐Ile levels increased dramatically after simulated herbivory in irJIH1, compared with wild‐type (WT) plants. When specialist (Manduca sexta) or generalist (Spodoptera littoralis) herbivores fed on irJIH1 plants they gained significantly less mass compared with those feeding on wild‐type (WT) plants. The poor larval performance was strongly correlated with the higher accumulation of several JA‐Ile‐dependent direct defense metabolites in irJIH1 plants. In the field, irJIH1 plants attracted substantially more Geocoris predators to the experimentally attached M. sexta eggs on their leaves, compared with empty vector plants, which correlated with higher herbivory‐elicited emissions of volatiles known to function as indirect defenses. We conclude that NaJIH1 encodes a new homeostatic step in JA metabolism that, together with JA and JA‐Ile‐hydroxylation and carboxylation of JA‐Ile, rapidly attenuates the JA‐Ile burst, allowing plants to tailor the expression of direct and indirect defenses against herbivore attack in nature.     

Plasticity in above‐ and belowground resource acquisition traits in response to single and multiple environmental factors in three tree species

Functional trait plasticity is a major component of plant adjustment to environmental stresses. Here, we explore how multiple local environmental gradients in resources required by plants (light, water, and nutrients) and soil disturbance together influence the direction and amplitude of intraspecific changes in leaf and fine root traits that facilitate capture of these resources. We measured population‐level analogous above‐ and belowground traits related to resource acquisition, i.e. “specific leaf area”–“specific root length” (SLA–SRL), and leaf and root N, P, and dry matter content (DMC), on three dominant understory tree species with contrasting carbon and nutrient economics across 15 plots in a temperate forest influenced by burrowing seabirds. We observed similar responses of the three species to the same single environmental influences, but partially species‐specific responses to combinations of influences. The strength of intraspecific above‐ and belowground trait responses appeared unrelated to species resource acquisition strategy. Finally, most analogous leaf and root traits (SLA vs. SRL, and leaf versus root P and DMC) were controlled by contrasting environmental influences. The decoupled responses of above‐ and belowground traits to these multiple environmental factors together with partially species‐specific adjustments suggest complex responses of plant communities to environmental changes, and potentially contrasting feedbacks of plant traits with ecosystem properties. We demonstrate that despite the growing evidence for broadly consistent resource‐acquisition strategies at the whole plant level among species, plants also show partially decoupled, finely tuned strategies between above‐ and belowground parts at the intraspecific level in response to their environment. This decoupling within species suggests a need for many species‐centred ecological theories on how plants respond to their environments (e.g. competitive/stress‐tolerant/ruderal and response‐effect trait frameworks) to be adapted to account for distinct plant‐environment interactions among distinct individuals of the same species and parts of the same individual.     

Induced Floral and Extrafloral Nectar Production Affect Ant‐pollinator Interactions and Plant Fitness

Thousands of plant species throughout tropical and temperate zones secrete extrafloral nectar to attract ants, whose presence provides an indirect defense against herbivores. Extrafloral nectaries are located close to flowers and may modify competition between ants and pollinators. Here, we used Lima bean (Phaseolus lunatus L.) to study the plants interaction between ants and flower visitors and its consequences for plant fitness. To test these objectives, we carried out two field experiments in which we manipulated the presence of ants and nectar production via induction with jasmonic acid (JA). We then measured floral and extrafloral nectar production, the number of patrolling ants and flower visitors as well as specific plant fitness traits. Lima bean plants under JA induction produced more nectar in both extrafloral nectaries and flowers, attracted more ants and produced more flowers and seeds than non‐induced plants. Despite an increase in floral nectar in JA plants, application of this hormone had no significant effects on flower visitor attraction. Finally, ant presence did not result in a decrease in the number of visits, but our results suggest that ants could negatively affect pollination efficiency. In particular, JA‐induced plants without ants produced a greater number of seeds compared with the JA‐treated plants with ants.     

Mechanisms and traits associated with compensation for defoliation in <Emphasis Type="Italic">Ruellia nudiflora</Emphasis>

A full understanding of the ecology and evolution of plant tolerance to damage requires the measurement of a diversity of traits (including multiple fitness-correlates) and underlying mechanisms. Here, we address the compensatory response to defoliation in the perennial herb Ruellia nudiflora, measure biomass allocation patterns and relate them to compensation, and address multiple mechanisms and traits that determine compensatory ability. We used maternal full-sib lines of R. nudiflora and conducted a defoliation experiment in which half the plants of each line were subjected to removal of 40% of leaf area (the other half remained undamaged). Fitness-correlated traits, physiological traits, and leaf longevity were measured during a 2-month period after defoliation. Using another set of plants, we conducted a second defoliation experiment and measured the concentration of non-structural carbohydrates to test for root-to-shoot carbon mobilization as a compensatory mechanism. R. nudiflora showed full compensation in terms of fruit output, and compensatory ability was positively correlated with investment in root biomass in the absence of damage. In addition, defoliated plants produced shorter-lived leaves and had a greater concentration of starch in roots, suggesting that reduced leaf longevity and accumulation of below-ground carbon reserves act as compensatory mechanisms. By measuring multiple fitness-correlates and induced traits, we provide a comprehensive evaluation of R. nudiflora compensatory responses to herbivory.     

Broccoli and turnip plants display contrasting responses to belowground induction by Delia radicum infestation and phytohormone applications

Induced responses to insect herbivory are a common phenomenon in the plant kingdom. So far, induced responses have mostly investigated in aerial plant parts. Recently it was found that root herbivore may also elicit both local and systemic responses affecting aboveground herbivores and their natural enemies. Using broccoli (Brassica oleracea subsp. italica L.) and turnip (Brassica rapa subsp. rapa L.), two cultivated brassicaceaous plants differing in their chemistry and morphology, we analysed the local and systemic induced responses triggered by Delia radicum L. damage, JA and SA application. We also assessed whether the root induction treatments affected D. radicum larval performance. Both D. radicum damage and JA induced changes in glucosinolate and sugar content as well as affected D. radicum performance, while SA application did not. Despite the uniform chemical responses, the effect on larval performance on broccoli and turnip plants was very different. On broccoli, JA root treatment reduced herbivore performance, whereas in turnips the same treatment enhanced it. JA- and D. radicum-induced responses followed similar patterns, which suggests that the JA signalling pathway is involved in root-induced responses to larval feeding. Glucosinolate induction cannot fully explain the differences found in the performance of D. radicum on the different species. Changes in other resistance factors might significantly contribute to the induced resistance in these brassicaceaeous species as well.     

Coping with herbivory: Photosynthetic capacity and resource allocation in two semiarid Agropyron bunchgrasses

Summary Agropyron desertorum, a grazing-tolerant bunchgrass introduced to the western U.S. from Eurasia, and Agropyron spicatum, a grazing-sensitive bunchgrass native to North America, were examined in the field for photosynthetic capacity, growth, resource allocation, and tiller dynamics. These observations allowed identification of physiological characteristics that may contribute to grazing tolerance in semiarid environments. A uniform matrix of sagebrush, Artemisia tridentata, provided an ecologically relevant competitive environment for both bunch-grass species. Physiological activity, growth, and allocation were also followed during recovery from a severe defoliation treatment and were correlated with tiller dynamics.Potential photosynthetic carbon uptake of both species was dominated by stems and leaf sheaths during June, when maximum uptake rates occurred. For both species, water use efficiency of stems and sheaths was similar to that of leaf blades, but nitrogen investment per photosynthetic surface area was less than in blades. In addition, soluble carbohydrates in stems and sheaths of both species constituted the major labile carbon pools in control plants. Contrary to current theory, these findings suggest that culms from which leaf blades have been removed should be of considerable value to defoliated bunchgrasses, and in the case of partial defoliation could provide important supplies of organic nutrients for regrowth. These interpretations, based on total pool sizes, differ markedly from previous interpretations based on carbohydrate concentrations alone, which suggested that crowns contain large carbohydrate reserves. In this study, crowns of both species contained a minor component of the total plant carbohydrate pool.Following defoliation, A. desertorum plants rapidly reestablished a canopy with 3 to 5 times the photosynthetic surface of A. spicatum plants. This difference was primarily due to the greater number of quickly growing new tillers produced following defoliation. Agropyron spicatum produced few new tillers following defoliation despite adequate moisture, and carbohydrate pools that were equivalent to those in A. desertorum.Leaf blades of regrowing tillers had higher photosynthetic capacity than blades on unclipped plants of both species, but the relative increase, considered on a unit mass, area, or nitrogen basis, was greater for A. desertorum than for A. spicatum. Agropyron desertorum also had lower investment of nitrogen and biomass per unit area of photosynthetic tissues, more tillers and leaves per bunch, and shorter lived stems, all of which can contribute to greater tolerance of partial defoliation.Greater flexibility of resource allocation following defoliation was demonstrated by A. desertorum for both nitrogen and carbohydrates. Relatively more allocation to the shoot system and curtailed root growth in A. desertorum resulted in more rapid approach to the preclipping balance between the root and shoot systems, whereas root growth in A. spicatum continued unabated following defoliation. Nitrogen required for regrowth in both species was apparently supplied by uptake rather than reserve depletion. Carbohydrate pools in the shoot system of both species remained very low following severe defoliation and were approximately equivalent to carbon fixed in one day by photosynthesis of the whole canopy.Dedicated to Drs. Michael Evenari and Konrad Springer     

Impact of growth form and carbohydrate reserves on tolerance to simulated deer herbivory and subsequent recovery in Liliaceae

? Premise of the study: Over-browsing of the understory vegetation by white-tailed deer has been a cause of decline in many plant populations. Liliaceae are particularly sensitive, yet individual species differ in their tolerance to deer herbivory. In this paper, we examine whether differences in clonal habit, carbon allocation patterns, and phenology influence the capacity of a species to tolerate and recover from repeated herbivory. ? Methods: Flowering ramets of Clintonia borealis, Maianthemum canadense, and Trillium erectum were subjected to total defoliation for one or two springs. ? Key results: Survival was highest in the nonclonal species, T. erectum, most probably due to its very large carbohydrate reserves. Nutrient reserves were less affected than carbohydrate reserves by defoliation, confirming the importance of carbohydrate reserves for survival. However, faster recovery following episodes of defoliation was observed not in the species that sprouted the earliest, T. erectum, but in the clonal species, M. canadense, which had the smallest carbohydrate reserves but also a lower shoot to root ratio than the other clonal species, C. borealis. All plants that were defoliated for 2 years only partially recovered in terms of leaf area, plant biomass, and carbohydrate and nutrient reserves, confirming the overall sensitivity of these species to simulated deer herbivory. ? Conclusions: High carbohydrate reserves and consequently low shoot to root ratios appear to increase tolerance to herbivory, whereas clonal species recover faster than nonclonal species. The role played by carbohydrates reserves suggests that these species could benefit from slightly higher light conditions in areas subjected to high deer pressure.