Herbivore-induced DMNT catalyzed by CYP82D47 plays an important role in the induction of JA-dependent herbivore resistance of neighboring tea plants.
Alkenes
/ metabolism
Animals
Camellia sinensis
/ genetics
Cloning, Molecular
Communication
Cyclopentanes
/ metabolism
Cytochrome P-450 Enzyme System
/ genetics
Gene Expression Regulation, Plant
Larva
Moths
Oxylipins
/ metabolism
Plant Defense Against Herbivory
Plant Growth Regulators
/ metabolism
Plant Proteins
/ genetics
Real-Time Polymerase Chain Reaction
Sequence Analysis, DNA
Volatile Organic Compounds
/ metabolism
CsCYP82D47
HIPVs
JA pathway
herbivorous insects
plant-plant communication
tea plant
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
revised:
21
07
2020
received:
31
03
2020
accepted:
24
07
2020
pubmed:
28
7
2020
medline:
27
8
2021
entrez:
27
7
2020
Statut:
ppublish
Résumé
Herbivore-induced plant volatiles play important ecological roles in defense against stresses. However, if and which volatile(s) are involved in the plant-plant communication in response to herbivorous insects in tea plants remains unknown. Here, plant-plant communication experiments confirm that volatiles emitted from insects-attacked tea plants can trigger plant resistance and reduce the risk of herbivore damage by inducing jasmonic acid (JA) accumulation in neighboring plants. The emission of six compounds was significantly induced by geometrid Ectropis obliqua, one of the most common pests of the tea plant in China. Among them, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) could induce the accumulation of JA and thus promotes the resistance of neighboring intact plants to herbivorous insects. CsCYP82D47 was identified for the first time as a P450 enzyme, which catalyzes the final step in the biosynthesis of DMNT from (E)-nerolidol. Down-regulation of CsCYP82D47 in tea plants resulted in a reduced accumulation of DMNT and significantly reduced the release of DMNT in response to the feeding of herbivorous insects. The first evidence for plant-plant communication in response to herbivores in tea plants will help to understand how plants respond to volatile cues in response to herbivores and provide new insight into the role(s) of DMNT in tea plants.
Substances chimiques
4,8-dimethyl-1,3,7-nonatriene
0
Alkenes
0
Cyclopentanes
0
Oxylipins
0
Plant Growth Regulators
0
Plant Proteins
0
Volatile Organic Compounds
0
jasmonic acid
6RI5N05OWW
Cytochrome P-450 Enzyme System
9035-51-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1178-1191Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Ali, M., Sugimoto, K., Ramadan, A., & Arimura, G.-i. (2013). Memory of plant communications for priming anti-herbivore responses. Scientific Reports, 3, 1872.
Ameye, M., Allmann, S., Verwaeren, J., Smagghe, G., Haesaert, G., Schuurink, R. C., & Audenaert, K. (2018). Tansley review green leaf volatile production by plants: A meta-analysis. New Phytologist, 220, 666-683.
Anderson R., Deb D., Withers J., He S.Y. & McDowell J. (2019) An oomycete RXLR effector triggers antagonistic plant hormone crosstalk to suppress host immunity. bioRxiv. https://doi.org/10.1101/561605.
Arimura, G.-i., Kopke, S., Kunert, M., Volpe, V., David, A., Brand, P., … Boland, W. (2008). Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiology, 146, 965-973.
Arimura, G. I., Matsui, K., & Takabayashi, J. (2009). Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factors and their ultimate functions. Plant and Cell Physiology, 50, 911-923.
Arimura, G. I., Ozawa, R., Shimoda, T., Nishloka, T., Boland, W., & Takabayashi, J. (2000). Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature, 406(6795), 512-515.
Bengtsson, M., Ba, A., Liblikas, I., Ramirez, M. I., Ansebo, L., Anderson, P., & Lo, J. (2001). Plant odor analysis of apple: Antennal response of codling moth females to apple volatiles during phenological development. Journal of Agricultural and Food Chemistry., 49(8), 3736-3741.
Blackmer, J. L., Byers, J. A., Shope, K. L., & Smith, J. P. (2004). Behavioral response of Lygus hesperus to conspeifics and headspace volatiles of alfalnay-tube olfactometer. Journal of Chemical Ecology., 30(8), 1547-1564.
Blanvillain, R., Wei, S., Wei, P., Kim, J. H., & Ow, D. W. (2011). Stress tolerance to stress escape in plants: Role of the OXS2 zinc-finger transcription factor family. The EMBO Journal, 30, 3812-3822.
Bolter, C. J., Dicke, M., Loon, J. J. A. V. A. N., & Visser, J. H. (1997). Herbivore-damaged plants during herbivory and after its termination. Journal of Chemical Ecology, 23, 1003-1023.
Bouwmeester, H., Schuurink, R. C., Bleeker, P. M., & Schiestl, F. (2019). The role of volatiles in plant communication. Plant Journal., 100, 892-907.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248-254.
Cai, X. M., Sun, X. L., Dong, W. X., Wang, G. C., & Chen, Z. M. (2014). Herbivore species, infestation time, and herbivore density affect induced volatiles in tea plants. Chemoecology, 24, 1-14.
Chen, Y., Guo, X., Gao, T., Zhang, N., Wan, X., Schwab, W., & Song, C. (2020). UGT74AF3 enzymes specifically catalyze the glucosylation of 4-hydroxy-2,5-dimethylfuran-3(2H)-one, an important volatile compound in Camellia sinensis. Horticulture Research, 7, 25.
Christensen, S. A., Nemchenko, A., Borrego, E., Murray, I., Sobhy, I. S., Boask, L., … Kolomiets, M. V. (2013). The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant Journal, 74(1), 59-73.
Dicke, M., Van Beek, T. A., Posthumus, M. A., Ben Dom, N., Van Bokhoven, H., & De Groot, A. (1990). Isolation and identification of volatile kairomone that affects acarine predatorprey interactions involvement of host plant in its production. Journal of Chemical Ecology., 16(2), 381-396.
Dong, F., Yang, Z., Baldermann, S., Sato, Y., Asai, T., & Watanabe, N. (2011). Herbivore-induced volatiles from tea (Camellia sinensis) plants and their involvement in intraplant communication and changes in endogenous nonvolatile metabolites. Journal of Agricultural and Food Chemistry, 59, 13131-13135.
Erb, M., Veyrat, N., Robert, C. A. M., Xu, H., Frey, M., Ton, J., & Turlings, T. C. J. (2015). Indole is an essential herbivore-induced volatile priming signal in maize. Nature Communications, 6, 6273.
Farmer, E. E., & Ryan, C. A. (1990). Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proceedings of the National Academy of Sciences of the United States of America., 87, 7713-7716.
Frost, C. J., Mescher, M. C., Carlson, J. E., & De Moraes, C. M. (2008). Plant defense priming against herbivores: Getting ready for a different battle. Plant Physiology, 146, 818-824.
Heil, M. (2014). Herbivore-induced plant volatiles: Targets, perception and unanswered questions. New Phytoogist, 204, 297-306.
Heil, M., & Karban, R. (2010). Explaining evolution of plant communicationby airborne signals. Trends in Ecology & Evolution, 25(3), 137-144.
Hu, L., Wu, Y., Wu, D., Rao, W., Guo, J., Ma, Y., … He, G. (2017). The coiled-coil and nucleotide binding domains of BROWN PLANTHOPPER RESISTANCE14 function in signaling and RESISTANCE against planthopper in rice. The Plant Cell, 29, 3157-3185.
Jing, T., Zhang, N., Gao, T., Zhao, M., Jin, J., Chen, Y., … Song, C. (2019). Glucosylation of (Z)-3-hexenol informs intraspecies interactions in plants: A case study in Camellia sinensis. Plant Cell and Environment, 42, 1352-1367.
Joo, Y., Goldberg, J. K., Chretien, L. T. S., Kim, S. G., Baldwin, I. T., & Schuman, M. C. (2019). The circadian clock contributes to diurnal patterns of plant indirect defense in nature. Journal of Integrative Plant Biology, 61, 924-928.
Karban, R., Wetzel, W. C., Shiojiri, K., Ishizaki, S., Ramirez, S. R., & Blande, J. D. (2014). Deciphering the language of plant communication: Volatile chemotypes of sagebrush. New Phytologist, 204, 380-385.
Karban, R., Wetzel, W. C., Shiojiri, K., Pezzola, E., & Blande, J. D. (2016). Geographic dialects in volatile communication between sagebrush individuals. Ecology, 2016(11), 97.
Karban, R., Yang, L. H., & Edwards, K. F. (2014). Volatile communication between plants that affects herbivory: A meta-analysis. Ecology Letters, 17, 44-52.
Lee, S., Badieyan, S., Bevan, D. R., Herde, M., Gatz, C., & Tholl, D. (2010). Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America., 107(49), 21205-21210.
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2CT method. Methods, 25(4), 402-408.
Lou, Y., Hua, X., Turlings, T. C. J., Cheng, J., Chen, X., & Ye, G. (2006). Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. Journal of Chemical Ecology, 32(11), 2375-2387.
Mas, F., Vereijssen, J., & Suckling, D. M. (2014). Influence of the pathogen Candidatus Liberibacter solanacearum on tomato host plant volatiles and psyllid vector settlement. Journal of Chemical Ecology., 40, 1197-1202.
Mccormick, A. C., Unsicker, S. B., & Gershenzon, J. (2012). The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends in Plant Science, 17, 303-310.
Meents, A. K. (2019). Volatile DMNT systemically induces jasmonate-independent direct anti-herbivore defense in leaves of sweet potato (Ipomoea batatas) plants. Scientific Reports, 9, 17431.
Mithöfer, A., & Boland, W. (2012). Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology, 63, 431-450.
O'Donnell, P. J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., & Bowles, D. J. (1996). Ethylene as a signal mediating the wound response of tomato plants. Science, 274(5294), 1914-1917.
Pickett, J. A., Woodcock, C. M., Midega, C. A. O., & Khan, Z. R. (2014). ScienceDirect push-pull farming systems. Current Opinion in Biotechnology, 26, 125-132.
Rajendran, S., Lin, I., Chen, M., Chen, C., & Yeh, K. (2014). Differential activation of sporamin expression in response to abiotic mechanical wounding and biotic herbivore attack in the sweet potato. BMC Plant Biology, 14, 111-121.
Richter, A., Schaff, C., Zhang, Z., Lipka, A. E., Tian, F., Tobias, G., … Buckler, E. S. (2016). Characterization of biosynthetic pathways for the production of the volatile homoterpenes DMNT and TMTT in Zea mays. Plant Cell, 28(10), 2651-2665.
Ruther, J., & Kleier, S. (2005). Plant-plant signaling: Ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. Journal of Chemical Ecology, 31, 2217-2222.
Scholz, S. S., Reichelt, M., Mekonnen, D. W., Ludewig, F., & Mithöfer, A. (2015). Insect herbivory-elicited GABA accumulation in plants is a wound-induced, direct, systemic, and jasmonate-independent defense response. Frontiers Plant Science, 6, 1128.
Shulaev, V., Silverman, P., & Raskin, I. (1997). Airborne signalling by methyl salicylate in plant pathogen resistance. Nature, 385, 718-721.
Song, C., Härtl, K., McGraphery, K., Hoffmann, T., & Schwab, W. (2018). Attractive but toxic: Emerging roles of Glycosidically bound volatiles and glycosyltransferases involved in their formation. Molecular Plant, 11, 1225-1236.
Staswick, P. E., & Tiryaki, I. (2004). The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell, 16, 2117-2127.
Su, J. W., Zeng, J. P., Qin, X. W., & Ge, F. (2009). Effect of needle damage on the release rate of Masson pine (Pinus massoniana) volatiles. Journal of Plant Research, 122(2), 193-200.
Sugimoto, K., Matsui, K., Iijima, Y., Akakabe, Y., Muramoto, S., Ozawa, R., … Takabayashi, J. (2014). Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. Proceedings of the National Academy of Sciences, 111, 7144-7149.
Sugimoto, K., Matsui, K., Takabayashi, J., Sugimoto, K., Matsui, K., & Takabayashi, J. (2015). Conversion of volatile alcohols into their glucosides in Arabidopsis. Communicative & Integrative Biology, 8(1), e992731.
Wang, S., Lan, Y., Chen, S., Chen, Y., & Yeh, K. (2002). Wound-response regulation of the sweet potato sporamin gene promoter region. Plant Molecular Biology., 48, 223-231.
Wang, X., Zeng, L., Liao, Y., Li, J., & Tang, J. (2019). Formation of α-Farnesene in tea (Camellia sinensis) leaves induced by herbivore-derived wounding and its effect on Neighboring tea plants. International Journal of Molecular Sciences, 20, 4151.
Wu, J., Hettenhausen, C., Meldau, S., & Baldwin, I. T. (2007). Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. The Plant Cell, 19, 1096-1122.
Yan, Z., & Wang, C. (2006). Wound-induced green leaf volatiles cause the release of acetylated derivatives and a terpenoid in maize. Phytochemistry, 67(1), 34-42.
Zeng, L., Liao, Y., Li, J., Zhou, Y., Tang, J., Dong, F., & Yang, Z. (2017). α-Farnesene and ocimene induce metabolite changes by volatile signaling in neighboring tea (Camellia sinensis) plants. Plant Science, 264, 29-36.
Zhang, P., Wei, J., Zhao, C., Zhang, Y., Li, C., Liu, S., & Dicke, M. (2019). Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles. Proceedings of the National Academy of Sciences of the United States of America, 116(15), 7387-7396.
Zhao, M., Wang, L., Wang, J., & Song, C. (2020). Induction of priming by cold stress via inducible volatile cues in neighboring tea plants. Journal of Integrative Plant Biology, 00(00), 1-8. https://doi.org/10.1111/jipb.12937
Zhao, M., Zhang, N., Gao, T., Jin, J., Jing, T., Wang, J., … Song, C. (2020). Sesquiterpene glucosylation mediated by glucosyltransferase UGT91Q2 is involved in the modulation of cold stress tolerance in tea plants. New Phytologist, 226, 362-372.