Arabidopsis thaliana plants are less resistant to attack by the generalist lepidopteran herbivore Trichoplusia ni when plants and herbivores are entrained to opposite, versus identical diurnal cycles and tested under ...Arabidopsis thaliana plants are less resistant to attack by the generalist lepidopteran herbivore Trichoplusia ni when plants and herbivores are entrained to opposite, versus identical diurnal cycles and tested under constant conditions. This effect is associated with circadian fluctuations in levels of jasmonic acid, the transcription factor MYC2, and glucosinolate contents in leaves. We tested whether a similar effect could be observed in a different plant-herbivore system： the wild tobacco Nicotiana attenuata and its co-evolved specialist herbivore, Manduca sexta. We measured larval growth on plants under both constant and diurnal conditions following identical or opposite entrainment, profiled the metabolome of attacked leaf tissue, quantified specific metabolites known to reduce M. sexta growth, and monitored A/I. sexta feeding activity under all experimental conditions. Entrainment did not consistently affect NI. sexta growth or plant defense induction. However, both were reduced under constant dark conditions,as was M. sexta feeding activity. Our data indicate that the response induced by NI. sexta in N. attenuata is robust to diurnal cues and independent of plant or herbivore entrain- ment. We propose that while the patterns of constitutive or general damage-induced defense may undergo circadian fluctuation, the orchestration of specific induced responses is more complex.展开更多
To defend themselves against herbivore attack, plants produce secondary metabolites, which are variously inducible and constitutively deployed, presumably to optimize their fitness benefits in light of their fitness c...To defend themselves against herbivore attack, plants produce secondary metabolites, which are variously inducible and constitutively deployed, presumably to optimize their fitness benefits in light of their fitness costs. Three phytohormones, jasmonates （JA） and their active forms, the JA-isoleucine （JA-Ile） and ethylene （ET）, are known to play central roles in the elicitation of induced defenses, but little is known about how this mediation changes over ontogeny. The Optimal Defense Theory （ODT） predicts changes in the costs and benefits of the different types of defenses and has been usefully extrapolated to their modes of deployment. Here we studied whether the herbivore-induced accumulation of JA, JA-Ile and ET changed over ontogeny in Nicotiana attenuata, a native tobacco in which inducible defenses are particularly well studied. Herbivore-elicited ET production changed dramatically during six developmental stages, from rosette through flowering, decreasing with the elongation of the first corollas during flower development. This decrease was largely recovered within a day after flower removal by decapitation. A similar pattern was found for the herbivore-induced accumulation of JA and JA-Ile. These results are consistent with ODT predictions and suggest that the last steps in floral development control the inducibility of at least three plant hormones, optimizing defense-growth tradeoffs.展开更多
The plant hormone jasmonic acid （JA） plays a central role in plant defense against herbivores. Herbivore damage elicits a rapid and transient JA burst in the wounded leaves and JA functions as a signal to mediate th...The plant hormone jasmonic acid （JA） plays a central role in plant defense against herbivores. Herbivore damage elicits a rapid and transient JA burst in the wounded leaves and JA functions as a signal to mediate the accumulation of various secondary metabolites that confer resistance to herbivores. Nicotiana attenuata is a wild tobacco species that inhabits western North America. More than fifteen years of study and its unique interaction with the specialist herbivore insect Manduca sexta have made this plant one of the best models for studying plant-herbivore interactions. Here we review the recent progress in understanding the elicitation of JA accumulation by herbivore-specific elicitors, the regulation of JA biosynthesis, JA signaling, and the herbivore-defense traits in N. attenuata.展开更多
DICER-like （DCL） proteins produce small RNAs that silence genes involved in development and defenses against viruses and pathogens. Which DCLs participate in plant-herbivore interactions remains unstudied. We identi...DICER-like （DCL） proteins produce small RNAs that silence genes involved in development and defenses against viruses and pathogens. Which DCLs participate in plant-herbivore interactions remains unstudied. We identified and stably silenced four distinct DCL genes by RNAi in Nicotiana attenuata （Torrey ex. Watson）, a model for the study of plant-herbivore interactions. Silencing DCL1 expression was lethal. Manduca sexta larvae performed significantly better on ir-dcl3 and ir-dcl4 plants, but not on ir-dcl2 plants compared to wild type plants. Phytohormones, defense metabolites and microarray analyses revealed that when DCL3 and DCL4 were silenced separately, herbivore resistance traits were regulated in distinctly different ways. Crossing of the lines revealed complex interactions in the patterns of regulation. Single ir-dcl4 and double ir-dcl2 ir-dcl3 plants were impaired in JA accumulation, while JA- Ile was increased in ir-dcl3 plants. Ir-dcl3 and ir-dcl4 plants were impaired in nicotine accumulation; silencing DCL2 in combination with either DCL3 or DCL4 restored nicotine levels to those of WT. Trypsin proteinase inhibitor activity and transcripts were only silenced in ir-dcl3 plants. We conclude that DCL2/3/4 interact in a complex manner to regulate anti-herbivore defenses and that these interactions significantly complicate the already challenging task of understanding smRNA function in the regulation of biotic interactions.展开更多
The superoxide （O^2-）-generating NADPH oxidases are crucial for the defense of plants against attack from pathogens; however, it remains unknown whether they also mediate responses against chewing insect herbivores....The superoxide （O^2-）-generating NADPH oxidases are crucial for the defense of plants against attack from pathogens; however, it remains unknown whether they also mediate responses against chewing insect herbivores. The transcripts of the respiratory burst NADPH oxidase homolog Narboh D in Nicotiana attenuate are rapidly and transiently elicited by wounding, and are amplified when Manduca sexta oral secretions （OS） are added to the wounds. The fatty-acid-amino-acid-conjugates （FACs）, demonstrably the major elicitors in M. sexta OS, are responsible for the increase in Narboh D transcripts. Silencing Narboh D significantly reduced reactive oxygen species （ROS） levels after OS elicitation, but neither OS-elicited jasmonic acid （JA） or JA-isoleucine （JA-Ile） bursts, pivotal hormones that regulates plant resistance to herbivores, nor early transcripts of herbivore defense-related genes （NaJAR4 and NaPAL1）, were influenced. However, late OS-elicited increases in trypsin proteinase inhibitors （TPIs）, as well as the transcript levels of defense genes such as polyphenol oxidase, TPI and Thionin were significantly reduced, in addition, Narboh D-silenced plants were more vulnerable to insect herbivores, especially the larvae of the generalist Spodoptera fittoralis. We thus conclude that Narboh D-based defenses play an important role in late herbivore-elicited responses.展开更多
Nearly half a century ago insect herbivores were found to induce the formation of green islands by manipulating cytokinin （CK） levels. However, the response of the CK pathway to attack by chewing insect herbivores r...Nearly half a century ago insect herbivores were found to induce the formation of green islands by manipulating cytokinin （CK） levels. However, the response of the CK pathway to attack by chewing insect herbivores remains unclear. Here, we characterize the CK pathway of Nicotiana attenuata （Torr. ex S. Wats.） and its response to wounding and perception of herbivoreassociated molecular patterns （HAMPs）. We identified 44 genes involved in CK biosynthesis, inactivation, degradation, and signaling. Leaf wounding rapidly induced transcriptional changes in multiple genes throughout the pathway, as well as in the levels of CKs, including isopentenyladenosine and cis-zeatin riboside; perception of HAMPs present in the oral secretions （OS） of the specialist herbivore Manduca sexta amplified these responses. The jasmonate pathway, which triggers many herbivore-induced processes, was not required for these HAMP-triggered changes, but rather suppressed the CK responses. Interestingly CK pathway changes were observed also in systemic leaves in response to wounding and OS application indicating a role of CKs in mediating long distance systemic processes in response to herbivory. Since wounding and grasshopper OS elicited similar accumulations of CKs in Arabidopsis thaliana L., we propose that CKs are integral components of wounding and HAMP-triggered responses in many plant species.展开更多
基金supported by funding from the Max Planck Society(all)the German Centre for Integrative Biodiversity Research(iDiv)Halle-Jena-Leipzig,funded by the German Research Foundation(FZT 118,M.C.S.)+2 种基金the Global Research Lab program(2012055546)from the National Research Foundation of Korea(Y.J.)a European Research Council advanced grant to I.T.B.(number 293926I.T.B.,M.C.S.,S.-G.K.,and S.M.)
文摘Arabidopsis thaliana plants are less resistant to attack by the generalist lepidopteran herbivore Trichoplusia ni when plants and herbivores are entrained to opposite, versus identical diurnal cycles and tested under constant conditions. This effect is associated with circadian fluctuations in levels of jasmonic acid, the transcription factor MYC2, and glucosinolate contents in leaves. We tested whether a similar effect could be observed in a different plant-herbivore system： the wild tobacco Nicotiana attenuata and its co-evolved specialist herbivore, Manduca sexta. We measured larval growth on plants under both constant and diurnal conditions following identical or opposite entrainment, profiled the metabolome of attacked leaf tissue, quantified specific metabolites known to reduce M. sexta growth, and monitored A/I. sexta feeding activity under all experimental conditions. Entrainment did not consistently affect NI. sexta growth or plant defense induction. However, both were reduced under constant dark conditions,as was M. sexta feeding activity. Our data indicate that the response induced by NI. sexta in N. attenuata is robust to diurnal cues and independent of plant or herbivore entrain- ment. We propose that while the patterns of constitutive or general damage-induced defense may undergo circadian fluctuation, the orchestration of specific induced responses is more complex.
文摘To defend themselves against herbivore attack, plants produce secondary metabolites, which are variously inducible and constitutively deployed, presumably to optimize their fitness benefits in light of their fitness costs. Three phytohormones, jasmonates （JA） and their active forms, the JA-isoleucine （JA-Ile） and ethylene （ET）, are known to play central roles in the elicitation of induced defenses, but little is known about how this mediation changes over ontogeny. The Optimal Defense Theory （ODT） predicts changes in the costs and benefits of the different types of defenses and has been usefully extrapolated to their modes of deployment. Here we studied whether the herbivore-induced accumulation of JA, JA-Ile and ET changed over ontogeny in Nicotiana attenuata, a native tobacco in which inducible defenses are particularly well studied. Herbivore-elicited ET production changed dramatically during six developmental stages, from rosette through flowering, decreasing with the elongation of the first corollas during flower development. This decrease was largely recovered within a day after flower removal by decapitation. A similar pattern was found for the herbivore-induced accumulation of JA and JA-Ile. These results are consistent with ODT predictions and suggest that the last steps in floral development control the inducibility of at least three plant hormones, optimizing defense-growth tradeoffs.
基金the Max Planck Society for financing the projects during our work at the Max Planck Institute for Chemical Ecologypart supported by the National Natural Science Foundation of China(Grant No.31201527) to L.Wang
文摘The plant hormone jasmonic acid （JA） plays a central role in plant defense against herbivores. Herbivore damage elicits a rapid and transient JA burst in the wounded leaves and JA functions as a signal to mediate the accumulation of various secondary metabolites that confer resistance to herbivores. Nicotiana attenuata is a wild tobacco species that inhabits western North America. More than fifteen years of study and its unique interaction with the specialist herbivore insect Manduca sexta have made this plant one of the best models for studying plant-herbivore interactions. Here we review the recent progress in understanding the elicitation of JA accumulation by herbivore-specific elicitors, the regulation of JA biosynthesis, JA signaling, and the herbivore-defense traits in N. attenuata.
基金the Max Planck Society for fundingSPP acknowledges support from MPG-DST India partner program
文摘DICER-like （DCL） proteins produce small RNAs that silence genes involved in development and defenses against viruses and pathogens. Which DCLs participate in plant-herbivore interactions remains unstudied. We identified and stably silenced four distinct DCL genes by RNAi in Nicotiana attenuata （Torrey ex. Watson）, a model for the study of plant-herbivore interactions. Silencing DCL1 expression was lethal. Manduca sexta larvae performed significantly better on ir-dcl3 and ir-dcl4 plants, but not on ir-dcl2 plants compared to wild type plants. Phytohormones, defense metabolites and microarray analyses revealed that when DCL3 and DCL4 were silenced separately, herbivore resistance traits were regulated in distinctly different ways. Crossing of the lines revealed complex interactions in the patterns of regulation. Single ir-dcl4 and double ir-dcl2 ir-dcl3 plants were impaired in JA accumulation, while JA- Ile was increased in ir-dcl3 plants. Ir-dcl3 and ir-dcl4 plants were impaired in nicotine accumulation; silencing DCL2 in combination with either DCL3 or DCL4 restored nicotine levels to those of WT. Trypsin proteinase inhibitor activity and transcripts were only silenced in ir-dcl3 plants. We conclude that DCL2/3/4 interact in a complex manner to regulate anti-herbivore defenses and that these interactions significantly complicate the already challenging task of understanding smRNA function in the regulation of biotic interactions.
文摘The superoxide （O^2-）-generating NADPH oxidases are crucial for the defense of plants against attack from pathogens; however, it remains unknown whether they also mediate responses against chewing insect herbivores. The transcripts of the respiratory burst NADPH oxidase homolog Narboh D in Nicotiana attenuate are rapidly and transiently elicited by wounding, and are amplified when Manduca sexta oral secretions （OS） are added to the wounds. The fatty-acid-amino-acid-conjugates （FACs）, demonstrably the major elicitors in M. sexta OS, are responsible for the increase in Narboh D transcripts. Silencing Narboh D significantly reduced reactive oxygen species （ROS） levels after OS elicitation, but neither OS-elicited jasmonic acid （JA） or JA-isoleucine （JA-Ile） bursts, pivotal hormones that regulates plant resistance to herbivores, nor early transcripts of herbivore defense-related genes （NaJAR4 and NaPAL1）, were influenced. However, late OS-elicited increases in trypsin proteinase inhibitors （TPIs）, as well as the transcript levels of defense genes such as polyphenol oxidase, TPI and Thionin were significantly reduced, in addition, Narboh D-silenced plants were more vulnerable to insect herbivores, especially the larvae of the generalist Spodoptera fittoralis. We thus conclude that Narboh D-based defenses play an important role in late herbivore-elicited responses.
基金funded by the Max-Planck-Society, Meza-Canales by the DAADVanková by the Czech Science Foundation, project no. 206/09/2062Meldau and Brütting are funded by Advanced Grant no. 293926 of the European Research Council to Baldwin
文摘Nearly half a century ago insect herbivores were found to induce the formation of green islands by manipulating cytokinin （CK） levels. However, the response of the CK pathway to attack by chewing insect herbivores remains unclear. Here, we characterize the CK pathway of Nicotiana attenuata （Torr. ex S. Wats.） and its response to wounding and perception of herbivoreassociated molecular patterns （HAMPs）. We identified 44 genes involved in CK biosynthesis, inactivation, degradation, and signaling. Leaf wounding rapidly induced transcriptional changes in multiple genes throughout the pathway, as well as in the levels of CKs, including isopentenyladenosine and cis-zeatin riboside; perception of HAMPs present in the oral secretions （OS） of the specialist herbivore Manduca sexta amplified these responses. The jasmonate pathway, which triggers many herbivore-induced processes, was not required for these HAMP-triggered changes, but rather suppressed the CK responses. Interestingly CK pathway changes were observed also in systemic leaves in response to wounding and OS application indicating a role of CKs in mediating long distance systemic processes in response to herbivory. Since wounding and grasshopper OS elicited similar accumulations of CKs in Arabidopsis thaliana L., we propose that CKs are integral components of wounding and HAMP-triggered responses in many plant species.
