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Chemical Manipulation of Abscisic Acid Signaling: a New Approach to Abiotic and Biotic Stress Management in Agriculture

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Chemical Manipulation of Abscisic Acid Signaling: a New Approach to Abiotic and Biotic Stress Management in Agriculture REVIEW www.advancedscience.com Chemical Manipulation of Abscisic Acid Signaling: A New Approach to Abiotic and Biotic Stress Management in Agriculture Kamalani Achala H. Hewage, Jing-Fang Yang, Di Wang, Ge-Fei Hao,* Guang-Fu Yang,* and Jian-Kang Zhu 1. Introduction The phytohormone abscisic acid (ABA) is the best-known stress signaling molecule in plants. ABA protects sessile land plants from biotic and abiotic Plant hormone structural analog may serve stresses. The conserved pyrabactin resistance/pyrabactin as a valuable starting point in develop- ing agrochemicals.[1,2] Because their natu- resistance-like/regulatory component of ABA receptors (PYR/PYL/RCAR) ral counterparts have been proven to be ca- perceives ABA and triggers a cascade of signaling events. A thorough pable of regulating plant metabolism struc- knowledge of the sequential steps of ABA signaling will be necessary for the tural analogs of plant hormones may have development of chemicals that control plant stress responses. The core superior performance to that of the natu- components of the ABA signaling pathway have been identified with adequate ral compounds. The first step in the devel- opment of plant hormone-based bioactive characterization. The information available concerning ABA biosynthesis, agents is the identification of the hormone transport, perception, and metabolism has enabled detailed functional studies signaling mechanism. The study of mech- on how the protective ability of ABA in plants might be modified to increase anisms underlying plant hormone signal- plant resistance to stress. Some of the significant contributions to chemical ing has greatly advanced over the past 10 manipulation include ABA biosynthesis inhibitors, and ABA receptor agonists years due to new developments in analytical and antagonists. Chemical manipulation of key control points in ABA chemistry, chemical biology, and biotech- nology. Five classical phytohormones,[3] in- signaling is important for abiotic and biotic stress management in agriculture. cluding auxin (AUX), ethylene (ET), gib- However, a comprehensive review of the current knowledge of chemical berellin (GA), cytokinin (CK), and abscisic manipulation of ABA signaling is lacking. Here, a thorough analysis of recent acid (ABA), have longbeen recognized as reports on small-molecule modulation of ABA signaling is provided. The regulators of many aspects of plant growth, challenges and prospects in the chemical manipulation of ABA signaling for plant development, and plant responses to stress. Although basic scientific research on the development of ABA-based agrochemicals are also discussed. the identification of plant hormone recep- tors has been conducted for many years, researchers are now finally discovering the mechanisms of hormone perception. With the elucidation of mechanisms underlying plant hormone perception, the K. A. H. Hewage, Dr. J.-F. Yang, D. Wang, Prof. G.-F. Hao, Prof. G.-F. Yang K. A. H. Hewage, Dr. J.-F. Yang, D. Wang, Prof. G.-F. Hao, Prof. G.-F. Yang Key Laboratory of Pesticide & Chemical Biology International Joint Research Center for Intelligent Biosensor Technology Ministry of Education and Health College of Chemistry Central China Normal University Central China Normal University Wuhan 430079, P. R. China Wuhan 430079, P. R. China Prof. G.-F. Yang E-mail: [email protected]; [email protected] Collaborative Innovation Center of Chemical Science and Engineering Tianjin 300072, P. R. China Prof. J.-K. Zhu Shanghai Center for Plant Stress Biology The ORCID identification number(s) for the author(s) of this article and CAS Center of Excellence in Molecular Plant Sciences can be found under https://doi.org/10.1002/advs.202001265 Chinese Academy of Sciences © 2020 The Authors. Published by Wiley-VCH GmbH. This is an open Shanghai 20032, P. R. China access article under the terms of the Creative Commons Attribution Prof. J.-K. Zhu License, which permits use, distribution and reproduction in any Department of Horticulture and Landscape Architecture medium, provided the original work is properly cited. Purdue University West Lafayette, IN 47907, USA DOI: 10.1002/advs.202001265 Adv. Sci. 2020, 7, 2001265 2001265 (1 of 40) © 2020 The Authors. Published by Wiley-VCH GmbH www.advancedsciencenews.com www.advancedscience.com development and use of plant hormone-based agrochemicals are becoming increasingly possible. Plant hormone-based agro- Ge-Fei Hao received his Ph.D. chemicals have a high probability of being perceived by plants degree in pesticide science because the complex metabolic network that perceives natural from Central China Normal hormones in plants is evolutionarily conserved. University (CCNU), China, in Agrochemical discovery guided by plant hormones is becom- 2011. He joined the College of ing increasingly important. Classical plant hormones[3,4] were Chemistry of CCNU in 2011 as discovered over 40 years ago, but a mechanistic understanding alecturerandbecameapro- of how plant cells perceive and translate hormone signals has fessor in 2015. His research remained a central question in plant biology. In the past decade, interests cover pesticide de- however, major classes of the plant hormone receptors have been sign, chem-bioinformatics, identified, and chemical signal transduction pathways from hor- and drug design. mone perception to response are currently being elucidated. This trend has provided a much clearer view of metabolic processes governed by plant hormones. As a result, the role of the plant hor- Guang-Fu Yang received his mones in agrochemical discovery is increasing. The reason for Ph.D. in pesticide science from this increase may be the need for a nongeneric active ingredient Nankai University, China, in that may be accepted by the general public as safe. The need for 1997. Then, he joined Institute new agrochemicals that may be effective over an extended period of Organic Synthesis of Cen- is also a priority for the agrochemical industry, and an agrochemi- tral China Normal University cal guided by natural phytohormones may satisfy the concern for (CCNU) as a lecturer and be- safety and long-term efficacy. came a professor in 2001. He Management of environmental stresses is essential for im- served as the Dean of College proved plant productivity, because biotic and abiotic stresses of Chemistry of CCNU (2001– significantly reduce crop growth and development. Agrochem- 2014), and as assistant pres- icals developed for crops have mainly functioned in the man- ident of CCNU (2014-2017). agement of biotic stressors, but both biotic and abiotic stress He is the current director of the factors trigger many responses in plants, which contribute to Key Laboratory of Pesticide & Chemical Biology (Ministry of the reduced yields. In response to a variety of biotic and abi- Education) from 2003 and the director of the International otic stresses, plants synthesize and release ABA. ABA, for ex- Joint Research Center for Intelligent Biosensor Technology ample, helps protect plants against extreme temperatures, re- and Health from 2018. His research interests cover pesticide duced or excessive water availability, high levels of salinity, discovery, chemical biology, and drug discovery. cold, high concentrations of heavy metals, and radiation. ABA also helps regulate many fundamental plant developmental pro- Jian-Kang Zhu is a distin- cesses such as seed development, root growth, senescence, and guished professor of plant [5-9] vegetative-reproductive phase transitions. In plants, natu- biology in the Departments of rally occurring ABA may simultaneously coordinate growth and Horticulture and Landscape [10] development and also adaptive stress responses. Therefore, Architecture and Biochem- the use of ABA-based agrochemicals could help crop plants istry at Purdue University. He manage environmental stress while maintaining acceptable obtained a doctoral degree in productivity. plant physiology from Purdue In recent years, ABA signaling in higher plants has been well- University. He was the Jane studied for the possibility of improving crop responses to abi- Johnson Chair Professor in [11,12] otic and biotic stresses via chemical manipulation. ABA’s the Institute for Integrative involvement in multiple and complex events in the plant life cy- Genome Biology and Depart- cle has attracted the attention of a diverse group of researchers, ment of Botany and Plant Sci- including plant physiologists, molecular biologists, and agricul- ences in the University of California, Riverside. His research tural chemists. The decoding of the ABA signaling pathway interests focus on understanding the molecular-genetic [13,14] was accelerated by the discovery of ABA receptors in 2009. mechanisms underlying plant resistance to salinity, drought, Researchers have now identified the core ABA signaling com- and low temperature stresses. ponents, including ABA receptor proteins (pyrabactin resis- tance/pyrabactin resistance-like/regulatory component of ABA receptors (PYR/PYL/RCAR) (hereafter referred to as PYLs), type 2C protein phosphatases (PP2Cs), and sucrose nonfermentation- Researchers have also developed some important chemi- 1 related subfamily of kinases (SnRK2s), as well as the down- cal modulators that target critical parts of the ABA signaling stream interacting proteins. Furthermore, the sequential events pathway. The sulfonamide compound quinabactin[5] acts as an of ABA perception and phenotypic responses have been con- effective ABA mimic for the ABA receptor and causes ABA-like firmed by
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