整合生物学期刊网

Plant Diversity >

2025 , Vol. 47 >Issue 04: 690 - 701

DOI: https://doi.org/10.1016/j.pld.2025.05.004

Articles

RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves

  • Che Zhan (展澈) ,
  • Na Xue (薛娜) ,
  • Zhongxiang Su (粟忠祥) ,
  • Tianyin Zheng (郑天胤) ,
  • Jianqiang Wu (吴建强)
展开
  • a. Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
    b. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China;
    c. State Key Laboratory of Plant Diversity and Specialty Crops, Beijing 100093, China

收稿日期: 2025-05-07

  修回日期: 2025-05-12

  网络出版日期: 2025-08-13

基金资助

This work was supported by National Natural Science Foundation of China (U23A20199), Yunnan Revitalization Talent Support Program “Yunling Scholar” and Yunnan Fundamental Research Projects (202201AS070056).

收起

RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves

  • Che Zhan (展澈) ,
  • Na Xue (薛娜) ,
  • Zhongxiang Su (粟忠祥) ,
  • Tianyin Zheng (郑天胤) ,
  • Jianqiang Wu (吴建强)
Expand
  • a. Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
    b. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China;
    c. State Key Laboratory of Plant Diversity and Specialty Crops, Beijing 100093, China

Received date: 2025-05-07

  Revised date: 2025-05-12

  Online published: 2025-08-13

Supported by

This work was supported by National Natural Science Foundation of China (U23A20199), Yunnan Revitalization Talent Support Program “Yunling Scholar” and Yunnan Fundamental Research Projects (202201AS070056).

Fold

摘要

Ca2+ signaling plays crucial roles in plant stress responses, including defense against insects. To counteract insect feeding, different parts of a plant deploy systemic signaling to communicate and coordinate defense responses, but little is known about the underlying mechanisms. In this study, micrografting, in vivo imaging of Ca2+ and reactive oxygen species (ROS), quantification of jasmonic acid (JA) and defensive metabolites, and bioassay were used to study how Arabidopsis seedlings regulate systemic responses in leaves after hypocotyls are wounded. We show that wounding hypocotyls rapidly activated both Ca2+ and ROS signals in leaves. RBOHD, which functions to produce ROS, along with two glutamate receptors GLR3.3 and GLR3.6, but not individually RBOHD or GLR3.3 and GLR3.6, in hypocotyls regulate the dynamics of systemic Ca2+ signals in leaves. In line with the systemic Ca2+ signals, after wounding hypocotyl, RBOHD, GLR3.3, and GLR3.6 in hypocotyl also cooperatively regulate the transcriptome, hormone jasmonic acid, and defensive secondary metabolites in leaves of Arabidopsis seedlings, thus controlling the systemic resistance to insects. Unlike leaf-to-leaf systemic signaling, this study reveals the unique regulation of wounding-induced hypocotyl-to-leaf systemic signaling and sheds new light on how different plant organs use complex signaling pathways to modulate defense responses.

关键词： Signal transduction; Grafting; Reactive oxygen species; Calcium signaling; Glutamate; Jasmonic acid

本文引用格式

Che Zhan (展澈) , Na Xue (薛娜) , Zhongxiang Su (粟忠祥) , Tianyin Zheng (郑天胤) , Jianqiang Wu (吴建强) . RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves[J]. Plant Diversity, 2025 , 47(04) : 690 -701 . DOI: 10.1016/j.pld.2025.05.004

Abstract

Ca2+ signaling plays crucial roles in plant stress responses, including defense against insects. To counteract insect feeding, different parts of a plant deploy systemic signaling to communicate and coordinate defense responses, but little is known about the underlying mechanisms. In this study, micrografting, in vivo imaging of Ca2+ and reactive oxygen species (ROS), quantification of jasmonic acid (JA) and defensive metabolites, and bioassay were used to study how Arabidopsis seedlings regulate systemic responses in leaves after hypocotyls are wounded. We show that wounding hypocotyls rapidly activated both Ca2+ and ROS signals in leaves. RBOHD, which functions to produce ROS, along with two glutamate receptors GLR3.3 and GLR3.6, but not individually RBOHD or GLR3.3 and GLR3.6, in hypocotyls regulate the dynamics of systemic Ca2+ signals in leaves. In line with the systemic Ca2+ signals, after wounding hypocotyl, RBOHD, GLR3.3, and GLR3.6 in hypocotyl also cooperatively regulate the transcriptome, hormone jasmonic acid, and defensive secondary metabolites in leaves of Arabidopsis seedlings, thus controlling the systemic resistance to insects. Unlike leaf-to-leaf systemic signaling, this study reveals the unique regulation of wounding-induced hypocotyl-to-leaf systemic signaling and sheds new light on how different plant organs use complex signaling pathways to modulate defense responses.

Key words： Signal transduction; Grafting; Reactive oxygen species; Calcium signaling; Glutamate; Jasmonic acid

参考文献

Bellandi, A., Papp, D., Breakspear, A., et al., 2022. Diffusion and bulk flow of amino acids mediate calcium waves in plants. Sci. Adv. 8, eabo6693.
Burow, M., Muller, R., Gershenzon, J., et al., 2006. Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis. J. Chem. Ecol. 32, 2333-2349.
Choi, J., Tanaka, K., Cao, Y., et al., 2014. Identification of a plant receptor for extracellular ATP. Science 343, 290-294.
Davletova, S., Schlauch, K., Coutu, J., et al., 2005. The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol. 139, 847-856.
Erb, M., Flors, V., Karlen, D., et al., 2009. Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J. 59, 292-302.
Erb, M., Reymond, P., 2019. Molecular interactions between plants and insect herbivores. Annu. Rev. Plant Biol. 70, 527-557.
Evans, M.J., Choi, W.G., Gilroy, S., et al., 2016. A ROS-Assisted Calcium Wave Dependent on the AtRBOHD NADPH Oxidase and TPC1 Cation Channel Propagates the Systemic Response to Salt Stress. Plant Physiol. 171, 1771-1784.
Farmer, E.E., Gasperini, D., Acosta, I.F., 2014. The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol. 204, 282-288.
Fichman, Y., Miller, G., Mittler, R., 2019. Whole-plant live imaging of reactive oxygen species. Mol. Plant 12, 1203-1210.
Fichman, Y., Mittler, R., 2021. Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants. Plant J. 107, 7-20.
Fichman, Y., Zandalinas, S.I., Peck, S., et al., 2022. HPCA1 is required for systemic reactive oxygen species and calcium cell-to-cell signaling and plant acclimation to stress. Plant Cell 34, 4453-4471.
Green, T.R., Ryan, C.A., 1972. Wound-induced proteinase inhibitor in plant leaves:a possible defense mechanism against insects. Science 175, 776-777.
Hu, C., Wu, S., Li, J., et al., 2022. Herbivore-induced Ca2+ signals trigger a jasmonate burst by activating ERF16-mediated expression in tomato. New Phytol. 236, 1796-1808.
Koo, A.J., Gao, X., Jones, A.D., et al., 2009. A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J. 59, 974-986.
Kumari, A., Chetelat, A., Nguyen, C.T., et al., 2019. Arabidopsis H+-ATPase AHA1 controls slow wave potential duration and wound-response jasmonate pathway activation. Proc. Natl. Acad. Sci. 116, 20226-20231.
Kwak, J.M., Mori, I.C., Pei, Z.M., et al., 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633.
Li, L., Li, C., Lee, G.I., et al., 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc. Natl. Acad. Sci. 99, 6416-6421.
Liu, B., Sun, L., Ma, L., et al., 2017. Both AtrbohD and AtrbohF are essential for mediating responses to oxygen deficiency in Arabidopsis. Plant Cell Rep. 36, 947-957.
Miller, G., Schlauch, K., Tam, R., et al., 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal 2, ra45.
Mittler, R., Zandalinas, S.I., Fichman, Y., et al., 2022. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol. 23, 663-679.
Moe-Lange, J., Gappel, N.M., Machado, M., et al., 2021. Interdependence of a mechanosensitive anion channel and glutamate receptors in distal wound signaling. Sci. Adv. 7, eabg4298.
Mousavi, S.A., Chauvin, A., Pascaud, F., et al., 2013. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500, 422-426.
Myers, R.J., Fichman, Y., Stacey, G., et al., 2022. Extracellular ATP plays an important role in systemic wound response activation. Plant Physiol. 189, 1314-1325.
Pearce, G., Strydom, D., Johnson, S., et al., 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895-897.
Setotaw, Y.B., Li, J., Qi, J.F., et al., 2024. Salicylic acid positively regulates maize defenses against lepidopteran insects. Plant Divers. 46, 519-529.
Shao, Q., Gao, Q., Lhamo, D., et al., 2020. Two glutamate-and pH-regulated Ca2+ channels are required for systemic wound signaling in Arabidopsis. Sci. Signal 13, eaba1453.
Tian, W., Wang, C., Gao, Q., et al., 2020. Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat. Plants 6, 750-759.
Toyota, M., Spencer, D., Sawai-Toyota, S., et al., 2018. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112-1115.
Tsutsui, H., Notaguchi, M., 2017. The use of grafting to study systemic signaling in plants. Plant Cell Physiol. 58, 1291-1301.
von Malek, B., van der Graaff, E., Schneitz, K., et al., 2002. The male-sterile mutant is defective in the gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216, 187-192.
Wang, L., Allmann, S., Wu, J., et al., 2008. Comparisons of LIPOXYGENASE3-and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol. 146, 904-915.
Wang, L., Einig, E., Almeida-Trapp, M., et al., 2018. The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nat. Plants 4, 152-156.
Waszczak, C., Carmody, M., Kangasjarvi, J., 2018. Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol. 69, 209-236.
Wittstock, U., Halkier, B.A., 2002. Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7, 263-270.
Wright, K.M., Oparka, K.J., 1996. The fluorescent probe HPTS as a phloem-mobile, symplastic tracer:An evaluation using confocal laser scanning microscopy. J. Exp. Bot. 47, 439-445.
Wu, J., Baldwin, I.T., 2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44, 1-24.
Wu, J., Hettenhausen, C., Meldau, S., et al., 2007. Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19, 1096-1122.
Xue, N., Zhan, C., Song, J., et al., 2022. The glutamate receptor-like 3.3 and 3.6 mediate systemic resistance to insect herbivores in Arabidopsis. J. Exp. Bot. 73, 7611-7627.
Zandalinas, S.I., Mittler, R., 2021. Vascular and nonvascular transmission of systemic reactive oxygen signals during wounding and heat stress. Plant Physiol. 186, 1721-1733.
Options
文章导航

/

〈 〉

版权所有 © 《Plant Diversity》编辑部
技术支持：北京玛格泰克科技发展有限公司