Ethylene mediates salicylic-acid-induced stomatal closure by controlling reactive oxygen species and nitric oxide production in Arabidopsis. (May 2020)

• Record Type: Journal Article
• Authors: Wang, Hui-Qin; Sun, Li-Ping; Wang, Li-Xiao; Fang, Xiao-Wei; Li, Zhong-Qi; Zhang, Fang-Fang; Hu, Xin; Qi, Cheng; He, Jun-Min
• Is Part Of: Plant science. Volume 294(2020)
• Publication Date: 2020-05
• Subjects: ABA abscisic acid -- ACC 1-aminocyclopropane-1-carboxylic acid -- ACS 1-aminocyclopropane-1-carboxylic acid synthase -- ARR2 ARABIDOPSIS RESPONSE REGULATOR 2 -- AVG aminoethoxyvinyl glycine -- BR brassinosteroid -- Col-0 Columbia-0 -- CPKs Ca2+-dependent protein kinases -- c-PTIO 2-(4-carboxyphenyl)-4, 4, 5, 5-tetramethylimidazoline-1-oxyl 3-oxide -- CTR1 CONSTITUTIVE TRIPLE RESPONSE1 -- DAF-2DA 4, 5-diaminofluorescein diacetate -- DPI diphenylene iodonium chloride -- EIN ETHYLENE INSENSITIVE -- ETR1 ETHYLENE RESPONSE 1 -- GUS β-Glucuronidase -- H2DCFDA 2′, 7′-dichlorofluorescin diacetate -- H2O2 hydrogen peroxide -- JAs jasmonates -- Ler Landsberg erecta -- MAPKs mitogen-activated protein kinases -- NO nitric oxide -- NOA1 NO associated protein 1 -- NPR1 NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 -- NR nitrate reductase -- PRX peroxidase -- RAN1 RESPONSE TO ANTAGONIST 1 -- ROS reactive oxygen species -- RT-PCR everse-transcription-PCR -- SA salicylic acid -- SHAM salicylhydroxamic acid -- SID2 SEPTUM INITIATION DEFFECTIVE 2 -- SNP sodium nitroprusside -- UV-B ultraviolet B; Ethylene -- NADPH oxidase -- Nitric oxide -- Reactive oxygen species -- Salicylic acid -- Stomatal closure; Botany -- Periodicals; Botanique -- Périodiques; 580
• DOI: 10.1016/j.plantsci.2020.110464
• Languages: English
• ISSNs: 0168-9452

Abstract

Highlights: NPR1 mediates SA-induced ethylene production by activating the expression of ACS2/6/11. Ethylene synthesis and signaling are required for SA-induced stomatal closure. ATRBOHD/F-generated ROS and NIA1/2-generated NO are required for SA guard cell signaling. Ethylene mediates SA-induced ROS in an RAN1-, ETR1- and CTR1-dependent manner. ROS mediates SA-induced NO through the ETR1, EIN2, EIN3 and ARR2-dependent pathway(s). Abstract: Both salicylic acid (SA) and ethylene induce stomatal closure and positively regulate stomatal immunity, but their interactions in guard cell signaling are unclear. Here, we observed that SA induced the expression of ethylene biosynthetic genes; the production of ethylene, reactive oxygen species (ROS) and nitric oxide (NO); and stomatal closure in Arabidopsis thaliana . However, SA-induced stomatal closure was inhibited by an ethylene biosynthetic inhibitor and mutations in ethylene biosynthetic genes, ethylene-signaling genes [ RESPONSE TO ANTAGONIST 1 ( RAN1 ), ETHYLENE RESPONSE 1 ( ETR1 ), ETHYLENE INSENSITIVE 2 ( EIN2 ), EIN3 and ARABIDOPSIS RESPONSE REGULATOR 2 ( ARR2 )], NADPH oxidase genes [ ATRBOHD and ATRBOHF ], and nitrate reductase genes ( NIA1 and NIA2 ). Furthermore, SA-triggered ROS production in guard cells was impaired in ran1, etr1, AtrbohD and AtrbohF, but not in ein2, ein3 or arr2 . SA-triggered NO production was impaired in all ethylene-signaling mutants tested and in nia1 and nia2 . The stomata of mutants for CONSTITUTIVE TRIPLE RESPONSE1 ( CTR1 ) showed constitutive ROS and NO production and closure. These results indicate that ethylene mediates SA-induced stomatal closure by activating ATRBOHD/F-mediated ROS synthesis in an RAN1-, ETR1- and CTR1-dependent manner. This in turn induces NIA1/2-mediated NO production and subsequent stomatal closure via the ETR1, EIN2, EIN3 and ARR2-dependent pathway(s).