Functional diversity of jasmonates in rice

Zheng Liu 0 Shumin Zhang 0 Ning Sun 3 Hongyun Liu 0 Yanhong Zhao 2 Yuling Liang 0 Liping Zhang 0 Yuanhuai Han 1 4 0 College of Life Sciences, Hebei University , Baoding , China 1 School of Agriculture, Shanxi Agricultural University , Taigu, Jinzhong , China 2 College of Agriculture, Ludong University , Yantai , China 3 The Affiliated School of Hebei Baoding Normal , Baoding , China 4 Key Laboratory of Crop Gene Resources and Germplasm Enhancement on Loess Plateau, Ministry of Agriculture , Taiyuan , China Phytohormone jasmonates (JA) play essential roles in plants, such as regulating development and growth, responding to environmental changes, and resisting abiotic and biotic stresses. During signaling, JA interacts, either synergistically or antagonistically, with other hormones, such as salicylic acid (SA), gibberellin (GA), ethylene (ET), auxin, brassinosteroid (BR), and abscisic acid (ABA), to regulate gene expression in regulatory networks, conferring physiological and metabolic adjustments in plants. As an important staple crop, rice is a major nutritional source for human beings and feeds one third of the world's population. Recent years have seen significant progress in the understanding of the JA pathway in rice. In this review, we summarize the diverse functions of JA, and discuss the JA interplay with other hormones, as well as light, in this economically important crop. We believe that a better understanding of the JA pathway will lead to practical biotechnological applications in rice breeding and cultivation. - Introduction Jasmonates (JA) are a class of polyunsaturated fatty acidderived phytohormones, playing important roles in plant growth and defense responses. The biosynthesis of JA initiates in chloroplasts, involving the release of -linolenic acid (-LeA, 18:3 or 18:2) from the lipid membrane by phospholipases (PLDs). Only -LeA (18:3) is utilized as a JA precursor through one of the seven distinct branches of the lipoxygenase (LOX) pathway, the allene oxide synthase (AOS) branch. Traditionally, -LeA (18:3) is oxidized by 13-LOX, an enzyme catalyzing regio- and stereo-specific dioxygenation of polyunsaturated fatty acid at C-13, to specifically form a fatty acid hydroperoxide, 13-HPOT (13S-hydroperoxy-(9Z,11E,15)-octadecatrienoic acid); however, the generation of both 9- and 13-hydroperoxides by OsLOX1 based on a dual C-9 and C-13 specificity was found in rice (Wang et al. 2008). The 13-HPOT then enters the seven enzymatic branches of the LOX pathway, including the oxidation by AOS to form an allene oxide, 12,13-EOT ((9Z,13S,15Z)-12,13-oxido-9,11,15-octadecatrienoic acid). The 12,13-EOT is unstable and can be cyclized by allene oxide cyclase (AOC) to form racemic 12-oxophytodienoic acid (12-OPDA). Subsequently, the cyclized OPDA is transferred from chloroplasts into peroxisomes, where it is reduced by OPDA reductase3 (OPR3) and three further -oxidation steps are conducted to produce (3R, 7S)-(+)-JA. After being released into the cytosol, it is converted into (3R, 7R)-()-JA, which can then be catalyzed by a jasmonate-amido synthase, JASMONATE RESISTANT 1 (JAR1), to form bioactive jasmonate (JA-Ile) by conjugating the amino acid isoleucine to (3R, 7R)-()-JA (Lyons et al. 2013; Svyatyna and Riemann 2012; Schaller and Stintzi 2009). Additionally, the hydroperoxy-octadecadienoic acids (HPOTs/HPODs) generated by LOXs can enter the hydroperoxide lyase (HPL) branch of the LOX pathway and are finally converted to green leaf volatiles (GLVs), which are indirectly involved in the defense against herbivores. Thus, the AOS and HPL branches compete for the same substrates and play antagonistic actions in rice (Chehab et al. 2007; Lyons et al. 2013). JA activates a succession of signaling pathways, resulting in the activation of the genes required for diverse functions, such as the regulation of plant growth and development (Browse 2009a,b), mediation of biotic and abiotic resistances (Browse 2009a, Santino et al. 2013), responses to different environmental conditions (Svyatyna and Riemann 2012), and crosstalk with other phytophormones (Vleesschauwer et al. 2013). Although most research on JA in plants was conducted in the model dicot plant Arabidopsis thaliana, significant progress has been made in recent years in rice (Oryza sativa), a monocot that is an important staple crop worldwide. Here, we review the diverse functions of JA in rice growth and development, environmental and abiotic responses, and pest and pathogen resistance as shown in Figure 1. Additionally, we highlight the importance of the interplay between JA and other hormones, as well as light, in rice. A functional comparison of the genes responsible for JA biosynthesis and signaling between rice and other plants, especially Arabidopsis is also provided (Table 1). Review Rice growth and development regulated by JA Sterility Flower development and sterility are effected by JA in plants, including Arabidopsis, tomato and maize (Wasternack and Hause 2013). In rice, a mitochondrial proteomic comparison between a sterile line and its fertile near-isogenic line revealed that a sex determination protein TASSEL SEED-2 (Os07g46920.1) was significantly up-regulated in the sterile line. At the same time, JA precursors were significantly increased in all of the developmental stages of the reproductive organs in the sterile line, except at the bicellular pollen stage, indicating that the biosynthetic levels of JA may regulate rice sterility (Liu et al. 2012a). The maize homologue of TASSELSEED-1 affects JA signaling, further confirming the effects of JA on rice flower development (Acosta et al. 2009). More direct evidence of JA functioning in rice sterility has been revealed by studying rice genes that are responsible for JA biosynthesis. Similar to the AOS knock-out mutants of Arabidopsis (Park et al. 2002), OsAOS1 and OsAOS2 RNAi-silenced transgenic rice plants show a severe or complete sterility phenotype during the reproductive stage (Bae et al. 2010). The rice OsOPR7 gene that is functionally similar to Arabidopsis opr3, which is involved in JA biosynthesis, is able to complement the male sterility phenotype of Arabidopsis opr3 mutants and restores JA production (Tani et al. 2008). Further, JA-deficient mutants, with a disrupted expression of OsAOC also show typical developmental phenotypes such as early flowering, elongated sterile lemma, and reduced fertility (Riemann et al. 2013). The over-production of JA is also thought to affect rice fertility. The oxylipin pathway contains several competing branch pathways, including allene oxide synthase (AOS) and hydroperoxide lyase (HPL), which are responsible for the production of JAs and aldehydes, respectively. Disruption of the rice HPL pathway by mutations results in a dramatic increase in JA production, leading to a reduced seed-setting ratio and a reduced tiller number due to the interference of pollen fertility (Liu et al. 2012b). These results ind (...truncated)