Oxylipins in plastidial retrograde signaling

Abstract

Oxylipins (compounds derived from the oxidation of polyunsaturated fatty acids) are essential in retrograde signaling emanating from plastids to the nucleus during plant developmental and stress responses. In this graphical review, we provide an overview of the chemical structure, biosynthesis and role of oxylipins, as both redox and hormonal signals, in controlling plant development and stress responses. We also briefly summarize current gaps in the understanding of the involvement of oxylipins in plastidial retrograde signaling to highlight future avenues for research.

Keywords: Chloroplasts; Jasmonates; Oxylipins; Plastids; ROS; Redox signaling.

Fig. 1

Plastids play a major role in the modulation of plant development and stress responses. (A) Plastids play a major role during plant development, including the regulation of root gravitropism (by sensing and signaling gravity with amyloplasts), photomorphogenesis (with the conversion of etioplasts to chloroplasts), harnessing and converting light energy into chemical energy in photosynthetic chloroplasts (capacity that is progressively lost during leaf senescence with the conversion of chloroplasts to gerontoplasts), and flower and fruit formation (with coloring chromoplasts for attraction). (B) Development and interconversion of plastids in plants. Proplastids can give rise to several plastids, not only including chloroplasts (with a photosynthesis function and that can give rise to gerontoplasts in senescing leaves), but also to storage plastids (such as amyloplasts and elaioplasts) and coloring plastids (chromoplasts) in flowers and fruits. Etioplasts are plastids that have developed in darkness (skotomorphogenesis).

Fig. 2

Schematic representation of oxylipin biosynthesis from chloroplastic polyunsaturated fatty acids (PUFA) triggered by abiotic stress. Reactive oxygen species (ROS) produced from excessive light at the reaction centers of chloroplast photosystems together with the excision of free fatty acids by lipases promote oxylipin formation, including reactive electrophile species (RES) and the jasmonic acid branch. Purple squares represent oxylipins with a described function in retrograde signaling under abiotic stress, while grey squares represent RES with putative signaling functions. AOC, allene oxide cyclase; AOS, allene oxide synthase; DHS, divinyl ether synthase; HPL, hydroperoxide liase; LOX, lipoxygenase; OPC-8, (1R, 2S)-3-oxo-2-[(Z)pent-2′-enyl]-cyclopentan-1-octanoic acid; OPDA, 12-oxo-phytodienoic acid; OPR, oxo-phytodienonate reductase. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3

Schematic representation of the role of oxylipins in the control of leaf senescence. Under optimal growing conditions (lower panel) leaves only produce small amounts of oxylipins as a result of low lipid peroxidation induced by mild levels of reactive oxygen species (ROS). Such conditions inhibit the jasmonic acid signaling pathway and JASMONATE ZIM-DOMAIN PROTEIN (JAZ) represses expression of MYC transcription factors, while low levels of lipid hydroperoxides and malondialdehyde (MDA) induce the production of antioxidants that enable ROS control in plant cells. During senescence (upper panel), jasmonic acid plays a prominent role in the activation of senescence-associated genes (SAGs) and expression of chlorophyll catabolic enzymes such as pheophorbide a (PAO1) that contribute to chlorophyll degradation and programmed cell death with a tight control of ROS production and oxylipin formation by antioxidant systems.

Fig. 4

Schematic representation of the oxylipin signaling pathways. Green lines represent hormonal pathways including the jasmonic acid branch, where jasmonyl isoleucine (JA-Ile) promotes JASMONATE ZIM-DOMAIN PROTEIN (JAZ) binding to the CORONATINE INSENSITIVE1 (COI1) and there is subsequently ubiquination and degradation of JAZ by the 26S proteasome, thereby inducing the expression of jasmonic acid (JA)-responsive genes. Several studies have reported COI1-independent pathways for OPDA signaling, including for the induction of the expression of several heat-shock proteins. Nevertheless, the COI1–JAZ receptor system could be modulated by OPDA with particular isoforms of COI1 and JAZ. On the other hand, the yellow lines represent the induction of RES-responsive genes in retrograde signalling by RES produced in chloroplast and mediated by protein and thiol/disulfide modifications. However, it remains elusive whether this RES could interact with other oxidative sensors such as EXECUTER1/2 (EX1/2) or 3′-phosphoadenosine 5′-phosphate (PAP) phosphatase SAL1 (SAL1). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)