12-Hydroxyjasmonic Acid Glucoside Causes Leaf-folding of Samanea Saman Through ROS Accumulation

Overview

Journal Sci Rep

Specialty Science

Date 2022 May 4

PMID 35508503

Authors

Gangqiang Yang

Yasuhiro Ishimaru

Shunji Hoshino

Yuki Muraoka

Nobuyuki Uozumi

Minoru Ueda

Affiliations

Soon will be listed here.

Abstract

Foliar nyctinasty, a circadian rhythmic movement in plants, is common among leguminous plants and has been widely studied. Biological studies on nyctinasty have been conducted using Samanea saman as a model plant. It has been shown that the circadian rhythmic potassium flux from/into motor cells triggers cell shrinking/swelling to cause nyctinastic leaf-folding/opening movement in S. saman. Recently, 12-hydroxyjasmonic acid glucoside (JAG) was identified as an endogenous chemical factor causing leaf-folding of S. saman. Additionally, SPORK2 was identified as an outward-rectifying potassium channel that causes leaf-movement in the same plant. However, the molecular mechanism linking JAG and SPORK2 remains elusive. Here, we report that JAG induces leaf-folding through accumulation of reactive oxygen species in the extensor motor cells of S. saman, and this occurs independently of plant hormone signaling. Furthermore, we show that SPORK2 is indispensable for the JAG-triggered shrinkage of the motor cell. This is the first report on JAG, which is believed to be an inactivated/storage derivative of JA, acting as a bioactive metabolite in plant.

References

Gorton H, Satter R . Extensor and Flexor Protoplasts from Samanea Pulvini : II. X-Ray Analysis of Potassium, Chlorine, Sulfur, Phosphorus, and Calcium. Plant Physiol. 1984; 76(3):685-90. PMC: 1064355. DOI: 10.1104/pp.76.3.685. View

Wrzaczek M, Brosche M, Kangasjarvi J . ROS signaling loops - production, perception, regulation. Curr Opin Plant Biol. 2013; 16(5):575-82. DOI: 10.1016/j.pbi.2013.07.002. View

Satter R, Geballe G, Applewhite P, Galston A . Potassium flux and leaf movement in Samanea saman. I. Rhythmic movement. J Gen Physiol. 1974; 64(4):413-30. PMC: 2226155. DOI: 10.1085/jgp.64.4.413. View

Forster S, Schmidt L, Kopic E, Anschutz U, Huang S, Schlucking K . Wounding-Induced Stomatal Closure Requires Jasmonate-Mediated Activation of GORK K Channels by a Ca Sensor-Kinase CBL1-CIPK5 Complex. Dev Cell. 2018; 48(1):87-99.e6. DOI: 10.1016/j.devcel.2018.11.014. View

Kleniewska P, Piechota A, Skibska B, Goraca A . The NADPH oxidase family and its inhibitors. Arch Immunol Ther Exp (Warsz). 2012; 60(4):277-94. DOI: 10.1007/s00005-012-0176-z. View

Ueda , Yamamura . Chemistry and Biology of Plant Leaf Movements. Angew Chem Int Ed Engl. 2000; 39(8):1400-1414. DOI: 10.1002/(sici)1521-3773(20000417)39:8<1400::aid-anie1400>3.0.co;2-z. View

Alvarez M, Pennell R, Meijer P, Ishikawa A, Dixon R, Lamb C . Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell. 1998; 92(6):773-84. DOI: 10.1016/s0092-8674(00)81405-1. View

Simon E, Satter R, Galston A . Circadian rhythmicity in excised samanea pulvini: I. Sucrose-white light interactions. Plant Physiol. 1976; 58(3):417-20. PMC: 542258. DOI: 10.1104/pp.58.3.417. View

Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J . ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 2003; 43(12):1473-83. DOI: 10.1093/pcp/pcf188. View

10.

Haroth S, Feussner K, Kelly A, Zienkiewicz K, Shaikhqasem A, Herrfurth C . The glycosyltransferase UGT76E1 significantly contributes to 12--glucopyranosyl-jasmonic acid formation in wounded leaves. J Biol Chem. 2019; 294(25):9858-9872. PMC: 6597828. DOI: 10.1074/jbc.RA119.007600. View

11.

Song Y, Miao Y, Song C . Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol. 2013; 201(4):1121-1140. DOI: 10.1111/nph.12565. View

12.

Ye W, Hossain M, Munemasa S, Nakamura Y, Mori I, Murata Y . Endogenous abscisic acid is involved in methyl jasmonate-induced reactive oxygen species and nitric oxide production but not in cytosolic alkalization in Arabidopsis guard cells. J Plant Physiol. 2013; 170(13):1212-5. DOI: 10.1016/j.jplph.2013.03.011. View

13.

Kwak J, Mori I, Pei Z, Leonhardt N, Torres M, Dangl J . NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 2003; 22(11):2623-33. PMC: 156772. DOI: 10.1093/emboj/cdg277. View

14.

Simon E, Satter R, Galston A . Circadian Rhythmicity in Excised Samanea Pulvini: II. Resetting the Clock by Phytochrome Conversion. Plant Physiol. 1976; 58(3):421-5. PMC: 542259. DOI: 10.1104/pp.58.3.421. View

15.

Kim T, Bohmer M, Hu H, Nishimura N, Schroeder J . Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol. 2010; 61:561-91. PMC: 3056615. DOI: 10.1146/annurev-arplant-042809-112226. View

16.

Murata Y, Pei Z, Mori I, Schroeder J . Abscisic acid activation of plasma membrane Ca(2+) channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 2001; 13(11):2513-23. PMC: 139468. DOI: 10.1105/tpc.010210. View

17.

Assmann S, Jegla T . Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO. Curr Opin Plant Biol. 2016; 33:157-167. DOI: 10.1016/j.pbi.2016.07.003. View

18.

Ueda M, Nakamura Y . Metabolites involved in plant movement and 'memory': nyctinasty of legumes and trap movement in the Venus flytrap. Nat Prod Rep. 2006; 23(4):548-57. DOI: 10.1039/b515708k. View

19.

Satter R, Guggino S, Lonergan T, Galston A . The effects of blue and far red light on rhythmic leaflet movements in samanea and albizzia. Plant Physiol. 1981; 67(5):965-8. PMC: 425810. DOI: 10.1104/pp.67.5.965. View

20.

Nakamura Y, Miyatake R, Ueda M . Enantiodifferential approach for the detection of the target membrane protein of the jasmonate glycoside that controls the leaf movement of Albizzia saman. Angew Chem Int Ed Engl. 2008; 47(38):7289-92. DOI: 10.1002/anie.200801820. View