Stem parasitic plant Cuscuta australis (dodder) transfers herbivory-induced signals among plants

Edited by Richard A. Dixon, University of North Texas, Denton, TX, and approved June 30, 2017 (received for review March 20, 2017)
July 24, 2017
114 (32) E6703-E6709

Significance

Cuscuta spp. (i.e., dodders) are plant parasites that connect to the vasculature of their host plants to extract water, nutrients, and even macromolecules. Knowledge of ecologically meaningful communications between host plants and Cuscuta, or between Cuscuta bridge-connected hosts, has remained obscure until now. Here we show that herbivore attack on one of the Cuscuta bridge-connected plants induces gene expression and increases the activity of trypsin proteinase inhibitors, and thus elevates the resistance to insects in other undamaged but Cuscuta-connected plants. This Cuscuta-mediated interplant signaling is rapid, conserved, far-reaching, and partly requires the plant hormone jasmonic acid. Although Cuscuta parasites can negatively influence their host plants, under certain circumstances, they may also provide ecologically relevant information-based benefits.

Abstract

Cuscuta spp. (i.e., dodders) are stem parasites that naturally graft to their host plants to extract water and nutrients; multiple adjacent hosts are often parasitized by one or more Cuscuta plants simultaneously, forming connected plant clusters. Metabolites, proteins, and mRNAs are known to be transferred from hosts to Cuscuta, and Cuscuta bridges even facilitate host-to-host virus movement. Whether Cuscuta bridges transmit ecologically meaningful signals remains unknown. Here we show that, when host plants are connected by Cuscuta bridges, systemic herbivory signals are transmitted from attacked plants to unattacked plants, as revealed by the large transcriptomic changes in the attacked local leaves, undamaged systemic leaves of the attacked plants, and leaves of unattacked but connected hosts. The interplant signaling is largely dependent on the jasmonic acid pathway of the damaged local plants, and can be found among conspecific or heterospecific hosts of different families. Importantly, herbivore attack of one host plant elevates defensive metabolites in the other systemic Cuscuta bridge-connected hosts, resulting in enhanced resistance against insects even in several consecutively Cuscuta-connected host plants over long distances (> 100 cm). By facilitating plant-to-plant signaling, Cuscuta provides an information-based means of countering the resource-based fitness costs to their hosts.

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Acknowledgments

This work was supported by Strategic Priority Research Program of the Chinese Academy of Sciences Grant XDB11050200 (to J.W.), Yunnan Recruitment Program of Experts in Sciences Grant 2012HA016 (to J.W.), a grant from the Max Planck Partner Group Program (to J.W.), National Natural Science Foundation of China Grants 31550110221 and 31650410652 (to C.H.), European Research Council Advanced Grant 293926 (to I.T.B.), and the Max Planck Society (I.T.B.).

Supporting Information

Supporting Information (PDF)
Dataset_S01 (XLSX)
Dataset_S02 (XLSX)
Dataset_S03 (XLSX)
Dataset_S04 (XLSX)
Dataset_S05 (XLSX)

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 32
August 8, 2017
PubMed: 28739895

Classifications

Submission history

Published online: July 24, 2017
Published in issue: August 8, 2017

Keywords

  1. Cuscuta
  2. parasitic plant
  3. systemic defense
  4. herbivore
  5. jasmonic acid

Acknowledgments

This work was supported by Strategic Priority Research Program of the Chinese Academy of Sciences Grant XDB11050200 (to J.W.), Yunnan Recruitment Program of Experts in Sciences Grant 2012HA016 (to J.W.), a grant from the Max Planck Partner Group Program (to J.W.), National Natural Science Foundation of China Grants 31550110221 and 31650410652 (to C.H.), European Research Council Advanced Grant 293926 (to I.T.B.), and the Max Planck Society (I.T.B.).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Christian Hettenhausen1
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Juan Li1
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Present address: College of Life Sciences, Southwest Forestry University, Kunming 650224, China.
Huifu Zhuang
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Huanhuan Sun
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Yuxing Xu
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Jinfeng Qi
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Jingxiong Zhang
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Yunting Lei
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Yan Qin
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Guiling Sun
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Present address: Department of Biology, Institute of Plant Stress Biology, State Key Laboratory of Cotton Biology, Henan University, Kaifeng 475004, China.
Lei Wang
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
Ian T. Baldwin
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena 07745, Germany
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;

Notes

4
To whom correspondence should be addressed. Email: [email protected].
Author contributions: C.H. and J.W. designed research; C.H., J.L., and H.S. performed research; C.H., J.L., H.Z., Y.X., J.Q., J.Z., Y.L., Y.Q., G.S., and L.W. analyzed data; C.H., I.T.B., and J.W. wrote the paper; and J.Z. made the illustrations.
1
C.H. and J.L. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Stem parasitic plant Cuscuta australis (dodder) transfers herbivory-induced signals among plants
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 32
    • pp. 8433-E6732

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