ABA receptor PYL9 promotes drought resistance and leaf senescence

Yang Zhao; Zhulong Chan; Jinghui Gao; Lu Xing; Minjie Cao; Chunmei Yu; Yuanlei Hu; Jun You; Haitao Shi; Yingfang Zhu; Yuehua Gong; Zixin Mu; Haiqing Wang; Xin Deng; Pengcheng Wang; Ray A. Bressan; Jian-Kang Zhu

doi:10.1073/pnas.1522840113

New Research In

Contributed by Jian-Kang Zhu, November 20, 2015 (sent for review October 16, 2015; reviewed by Hillel Fromm and Tuan-Hua David Ho)

Significance

We identified transgenic plants that are extremely resistant to drought from a large-scale screening of transgenic plants overexpressing the pyrabactin resistance 1-like (PYL) family of abscisic acid (ABA) receptors. We explored how these plants resist drought by examining both short-term responses, such as stomatal closure, and long-term responses, such as senescence. The physiological roles of ABA-induced senescence under stress conditions and the underlying molecular mechanism are unclear. Here, we found that ABA induces senescence by activating ABA-responsive element-binding factors and Related to ABA-Insensitive 3/VP1 transcription factors through core ABA signaling. Our results suggest that PYL9 promotes drought resistance by not only limiting transpirational water loss but also, causing summer dormancy-like responses, such as senescence, in old leaves and growth inhibition in young tissues under severe drought conditions.

Abstract

Drought stress is an important environmental factor limiting plant productivity. In this study, we screened drought-resistant transgenic plants from 65 promoter-pyrabactin resistance 1-like (PYL) abscisic acid (ABA) receptor gene combinations and discovered that pRD29A::PYL9 transgenic lines showed dramatically increased drought resistance and drought-induced leaf senescence in both Arabidopsis and rice. Previous studies suggested that ABA promotes senescence by causing ethylene production. However, we found that ABA promotes leaf senescence in an ethylene-independent manner by activating sucrose nonfermenting 1-related protein kinase 2s (SnRK2s), which subsequently phosphorylate ABA-responsive element-binding factors (ABFs) and Related to ABA-Insensitive 3/VP1 (RAV1) transcription factors. The phosphorylated ABFs and RAV1 up-regulate the expression of senescence-associated genes, partly by up-regulating the expression of Oresara 1. The pyl9 and ABA-insensitive 1-1 single mutants, pyl8-1pyl9 double mutant, and snrk2.2/3/6 triple mutant showed reduced ABA-induced leaf senescence relative to the WT, whereas pRD29A::PYL9 transgenic plants showed enhanced ABA-induced leaf senescence. We found that leaf senescence may benefit drought resistance by helping to generate an osmotic potential gradient, which is increased in pRD29A::PYL9 transgenic plants and causes water to preferentially flow to developing tissues. Our results uncover the molecular mechanism of ABA-induced leaf senescence and suggest an important role of PYL9 and leaf senescence in promoting resistance to extreme drought stress.

Footnotes

↵¹Y. Zhao and Z.C. contributed equally to this work.
↵²To whom correspondence should be addressed. Email: jkzhu{at}purdue.edu.

Author contributions: Y. Zhao, Z.C., and J.-K.Z. designed research; Y. Zhao, Z.C., J.G., L.X., M.C., C.Y., Y.H., J.Y., H.S., Y. Zhu, Y.G., Z.M., H.W., and X.D. performed research; Y. Zhao, Z.C., M.C., P.W., R.A.B., and J.-K.Z. analyzed data; and Y. Zhao, Z.C., R.A.B., and J.-K.Z. wrote the paper.
Reviewers: H.F., Tel Aviv University; and T.-H.D.H., Academia Sinica.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1522840113/-/DCSupplemental.

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