Molecular interaction of jasmonate and phytochrome A signalling

Journal of Experimental Botany, Vol. 65, No. 11, pp. 2847–2857, 2014 doi:10.1093/jxb/eru230 Advance Access publication 28 May, 2014 Review Paper Molecular interaction of jasmonate and phytochrome A signalling Hsu-Liang Hsieh1 and Haruko Okamoto2,3,* 1 2 * To whom correspondence should be addressed. E-mail: Received 7 January 2014; Revised 17 April 2014; Accepted 28 April 2014 Abstract The phytochrome family of red (R) and far-red (FR) light receptors (phyA–phyE in Arabidopsis) play important roles throughout plant development and regulate elongation growth during de-etiolation and under light. Phytochromes regulate growth through interaction with the phytohormones gibberellin, auxin, and brassinosteroid. Recently it has been established that jasmonic acid (JA), a phytohormone for stress responses, namely wounding and defence, is also important in inhibition of hypocotyl growth regulated by phyA and phyB. This review focuses on recent advances in our understanding of the molecular basis of the interaction between JA and phytochrome signalling particularly during seedling development in Arabidopsis. Significantly, JA biosynthesis genes are induced by phyA. The protein abundance of JAR1/FIN219, an enzyme for the final synthesis step to give JA-Ile, an active form of JA, is also determined by phyA. In addition, JAR1/FIN219 directly interacts with an E3-ligase, COP1, a master regulator for transcription factors regulating hypocotyl growth, suggesting a more direct role in growth regulation. There are a number of points of interaction in the molecular signalling of JA and phytochrome during seedling development in Arabidopsis, and we propose a model for how they work together to regulate hypocotyl growth. Key words: Jasmonic acid (JA), low R:FR light, photomorphogenesis, phytochrome, shade avoidance syndrome, skotomorphogenesis. Introduction Global food security has become one of the major concerns in recent years, and understanding plant photomorphogenesis is as important as ever for producing further yield increases for crop species. Photomorphogenesis is a lightregulated developmental programme that controls most aspects of plant development including the regulation of plant architecture (Fankhauser and Chory, 1997). Plants grown in the light typically have short and robust stems with dark-green leaves. In contrast, plants grown in darkness undergo a skotomorphogenic growth strategy and have elongated stems and yellow, etiolated cotyledons or leaves. Plants grown under shade have a morphology that is more akin to that of skotomophogenic growth and have paler leaves with an elongated and weaker stature as they seek to grow taller than their neighbouring plants. This type of response is unfavourable in crop species grown under controlled monocultures in modern agriculture as energy is allocated away from tissues for harvest. For example, >75% of the yield increase in commercial maize hybrids released between 1955 and 2000 is associated with increased tolerance to such competition from neighbours (Duvick, 2005). Plant responses to shade are not only caused by the reduced level of available light energy, but are primarily due to an enrichment of far-red (FR) light reflecting off neighbouring leaves and stems. Plants have a number of photoreceptors such as UV RESISTANCE LOCUS 8 (UVR8), cryptochromes, © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: 3 Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei, Taiwan Centre for Biological Sciences, University of Southampton, Southampton, UK Department of Biochemistry, Faculty of Pharmaceutical Sciences, Iwate Medical University, Iwate, Japan 2848 | Hsieh and Okamoto focused on the molecular interactions between JA and phyA signalling in photomorphogenesis. JA in photomorphogenesis Active JAs in phytochrome-dependent hypocotyl growth regulation JA is synthesized from α-linoleic acid in the plastid thylakoid membrane (Fig. 1) by lipoxygenases (LOXs), allene oxide synthases (AOSs), and allene oxide cyclases (AOCs), to give 12-oxophytodienoic acid (OPDA). OPDA is then imported into the peroxisome by the ABC transporter, COMATOSE (CTS1) (Theodoulou et al., 2005), is oxidized by oxophytodienoic acid reductase 3 (OPR3), and undergoes three cycles of β-oxidization. The resulting JA is either modified by hydroxylation at the alkyl moiety to permit conjugation with a sugar or sulphate group or, alternatively, is modified at Fig. 1. JA biosynthesis pathway in Arabidopsis. JA is synthesized from α-linoleic acid in the chloroplast thylakoid membrane via nuclear genes encoding JA biosynthesis enzymes such as LOX (lipoxygenase), AOS (allene oxide synthase), and AOC (allene oxide cyclase). The JA intermediate 12-oxophytodienoic acid (OPDA) is transported into the peroxisome where it is further processed by β-oxidation. Finally, JA (jasmonic acid) is conjugated with isoleucine by an acyl acid amino synthase, JAR1/FIN219. MeJA, JA-ACC, 12-O-Glc-JA, and JA-O-Glc are all reported to be biologically active. phototropins, and phytochromes which between them are capable of perceiving light wavelengths ranging from UV-B to FR light (Devlin et al., 2007; Casal, 2013). The blue light photoreceptors, the cryptochromes (Keller et al., 2011) and phototropins (Casal, 2013), are important in perceiving the reduced level of available light energy in shade. The red (R) and FR light receptor phytochromes are the major photoreceptors for plants in perception of the R:FR ratio of light under canopy shade. The plant genome encodes a family of phytochrome genes (i.e. PHYA–PHYE in Arabidopsis) and the encoded proteins bind to an open tetrapyrrole chromophore, phytochromobilin (Franklin and Quail, 2010). The resulting holoprotein photoreversibly absorbs R and FR light and, to a simple approximation, the R:FR ratio of the light environment is translated to the molecular ratio of R and FR lightabsorbing forms of phytochrome. Mutant studies have shown that phytochrome B (phyB) is the primary photoreceptor for R light in growth inhibition regulation of the embryonic stem, the ‘hypocotyl’, while that for FR light is phytochrome A (phyA). Long hypocotyl mutant screening under monochromatic R and FR light has identified the function of a number of signalling molecules downstream of both phyA and phyB. The molecular basis of phytochrome signalling has been covered comprehensively by a number of excellent reviews (Bae and Choi, 2008; Franklin and Quail, 2010). The plant hormones gibberellin (de Lucas et al., 2008; Feng et al., 2008; Lau and Deng, 2010), auxin (Tao et al., 2008; Halliday et al., 2009; Franklin et al., 2011), and brassinosteroids (Bai et al., 2012; Oh et al., 2012) have all been found to be important in regulating photomorphogenesis (de Lucas and Prat, 2014). In addition, a newer member of the phytohormo (...truncated)