Organelles and phytohormones: a network of interactions in plant stress responses

Abstract

Phytohormones are major signaling components that contribute to nearly all aspects of plant life. They constitute an interconnected communication network to fine-tune growth and development in response to the ever-changing environment. To this end, they have to coordinate with other signaling components, such as reactive oxygen species and calcium signals. On the one hand, the two endosymbiotic organelles, plastids and mitochondria, control various aspects of phytohormone signaling and harbor important steps of hormone precursor biosynthesis. On the other hand, phytohormones have feedback actions on organellar functions. In addition, organelles and phytohormones often act in parallel in a coordinated matter to regulate cellular functions. Therefore, linking organelle functions with increasing knowledge of phytohormone biosynthesis, perception, and signaling will reveal new aspects of plant stress tolerance. In this review, we highlight recent work on organelle-phytohormone interactions focusing on the major stress-related hormones abscisic acid, jasmonates, salicylic acid, and ethylene.

Keywords: Abscisic acid (ABA); chloroplast; ethylene; jasmonates; mitochondria; phytohormones; plant organelles; plastids; retrograde signaling; salicylic acid (SA); stress signaling.

Fig. 1.

The chloroplast as metabolic hub for phytohormone precursors. Numerous phytohormone pathways start with secondary metabolism in plastids: xanthoxine biosynthesis via the xanthophyll cycle—the precursor of ABA; chorismate biosynthesis—the precursor of SA and auxin (IAA); oxidized lipids such as linolenic acid—the precursor of jasmonates (via JA); cystathionine—the precursor for methionine and thus ethylene. ACC: 1-aminocyclopropane 1-carboxylate; IAA, indole-3-acetic acid; OPDA, oxophytodienoic acid; SAM, S-adenosyl-l-methionine.

Fig. 2.

Direct/indirect signals in regulation of gene expression. Different types of connections between organelles and hormone signaling affect gene expression. (A) Direct signals: hormone levels, depending on precursor metabolites for hormone biosynthesis of exclusive organellar origin, regulate a subset of genes (yellow) while another subset of genes is controlled by retrograde signals from organelles (green), and a third subset of genes is regulated by both input pathways (blue). (B) Indirect signals: hormone levels regulating a subset of genes are indirectly altered via second messenger molecules of organellar origin, modulating the enzymes relevant for hormone biosynthesis. (C) Other signaling connections: transcriptional changes that do not fall into (A, B) but require a functional hormonal signaling cascade and a functional organellar retrograde signaling cascade at the same time.

Fig. 3.

The role of organelles in abscisic acid (ABA) signaling. ABA biosynthesis is initiated in chloroplasts by the non-mevalonate (MEP⁻) pathway and continuous via phytoene, lycopene, β-carotene, and zeaxanthin biosynthesis. The xanthophyll cycle converts zeaxanthin into violaxanthin, which is converted into xanthoxin. In the cytosol, xanthoxin is the substrate for the synthesis of ABA aldehyde and finally ABA. ABA is perceived through receptors from the RCAR/PYR/PYL family and PP2C co-receptors, which in turn activate SnRK2s and ABFs by phosphorylation. Chloroplast signals and functions, such as the SAL–PAP pathway and NPQ, control ABA biosynthesis and signaling. AAO, ABA-aldehyde oxidase; ABF, ABA responsive element-binding factor; LHY, late hypocotyl elongation factor; NCED, 9-cis-epoxycarotenoid dioxygenase; NPQ, non-photochemical quenching; PAP, 3ʹ-phosphoadenosine-5ʹ-phosphate; PP2C, protein phosphatase 2C; SAL1, dinucleotide phosphatase/inositol phosphate phosphatase; SDR, short chain dehydrogenase; SLAC1, slow anion channel-associated 1; SnRK2s, SNF1-related protein kinases; VDE, violaxanthin de-epoxidase; XRN, exoribonucleases; ZEP, zeaxanthin epoxidase.

Fig. 4.

The role of organelles in jasmonate signaling. The term jasmonate comprises JA and JA-Ile as well as several precursors and catabolic derivatives some of which also possess bioactivity. Jasmonate biosynthesis is initiated in chloroplasts by oxidation of C18:3 (octadecanoid pathway) and C16:3 (hexadecanoid pathway) fatty acids derived from galactolipids, which are converted in several steps to the first committed precursor, OPDA. The MDGD/DGDG ratio, but also conjugation of OPDA to GSH or esterification to galactolipids (arabidopsides), affects OPDA homeostasis. Biosynthesis of JA continues in peroxisomes by β-oxidation of OPC-8:0 and OPC-6:0. A minor, less well described bypass pathway of JA formation involves tnOPDA and 4,5-ddh-JA. JA-Ile, the most bioactive of the jasmonates, is finally synthesized in the cytosol from JA and isoleucine, the latter being derived from methionine also made in chloroplasts. Ultimately, JA-Ile exerts its action in the nucleus by promoting the formation of SCF^COI1–JAZ co-receptor complexes and thus releasing JAZ-dependent gene suppression. 4,5ddh-JA, 4,5-didehydro-jasmonate; 10,11-EHT, 10,11(S)-epoxy-hexadecatrienoic acid; 11-HPHT, 11(S)-hydroperoxy-hexadecatrienoic acid; 12,13-EOT, 12,13(S)-epoxy-octadecatrienoic acid; 13-HPOT, 13(S)-hydroperoxylinolenic acid; α-LEA, α-linolenic acid; AOC, allene oxide cyclase; AOS, allene oxide synthase; DGDG, digalactosyl-diacylglycerol; GH3.10, glycoside hydrolase 3 gene family 10; HPL, hydroperoxide lyase; JA, jasmonic acid; JA-Glc, glycosylated jasmonate; JAR1, jasmonate-resistant 1; JASSY, chloroplast jasmonate transporter; LOX, lipoxygenases; MeJA, methyl jasmonate; MGDG, monogalactosyldiacylglycerol; OPC, 3-oxo-2-(2⁰-[Z]-pentenyl)-cyclopentane-1-octanoic acid; OPCL1, OPC-8:0 CoA ligase 1; OPDA, oxophytodienoic acid; OPR, OPDA reductase; PXA1, peroxisomal ABC-transporter 1.

Fig. 5.

The role of organelles in ethylene signaling. The chloroplast-localized enzyme cystathionine γ-synthase (CGS) catalyses the formation of cystathionine (CysT) from cysteine (Cys) and O-phosphohomoserine (OPH). Cystathionine is further transformed into homocysteine (Hcy) by cystathionine β-lyase (CBL). In the next step, the chloroplast-localized isoform of the methionine synthase 3 (MS3) forms methionine (Met), which in turn is transported out of the chloroplasts by SAMC1. In the cytoplasm Met is directly transformed into S-adenosylmethionine (SAM) by S-adenosylmethionine synthase (SAMS). SAM as main methyl donor is transported also back to the chloroplast by SAMC1. In the cytoplasm, SAM is converted into 1-aminocyclopropane 1-carboxylate (ACC) by the rate limiting ACC synthases (ACSs). After phosphorylation by calcium-dependent kinases (CDPK) and/or MAP kinases (MPK), ACSs are stabilized and therefore activated. Dephosphorylation of ACSs by different protein phosphatases (PP2A, PP2C) destabilizes the protein and leads to an immediate loss of ACS activity. The by-product of the reaction conducted by ACS, 5ʹ-methylthioadenosine (MTA), enters the Yang cycle to be detoxified and recycled into Met. ACC oxidase (ACO) catalyses the final step from ACC to ethylene. The mitonuclear protein imbalance leads to increase of mitochondrial reactive oxygen species (ROS) level. As a consequence, the mitochondrial unfolded protein response (UPRmt) is initiated. The elevated ROS level activates MPK6, which in turn promotes ET production by two ways: by phosphorylation of ACS6 and increase in transcription of the ACS6 gene. Additionally, nuclear ETHYLENE INSENSITIVE 3 (EIN3), a major ethylene responsive transcription factor, also plays a part in anterograde signaling (dashed line) in the chloroplast. After dark to light transition, PHYB promotes EIN3 and PIF3 degradation leading to LHCA and LHCB expression and chloroplast development.

Fig. 6.

The role of organelles in salicylic acid signaling. Overview of salicylic acid (SA) synthesis via the isochorismate synthase (ICS) and phenylalanine ammonia-lyase (PAL) pathways starting from chorismate. ICS converts chorismate into isochorismate (IC) in plastids. EDS5 exports IC from the plastid into the cytosol where PBS3 converts it into isochorismoyl-9-glutamate and further into SA by EPS1. The PAL pathway converts chorismate into prephenate by CM1 or CM2. Prephenate is converted into arogenate by PPA-AT and further to tyrosine by ADH or phenylalanine by ADT. CM1, ADH, and ADT are negatively regulated by their corresponding amino acid products. Tyrosine and phenylalanine are transported into the cytosol where PPY-AT converts them to phenylalanine. Phenylalanine produced from both plastidal and cytosolic pathways is further converted into trans-cinnamic acid by PAL and then into SA via ortho-coumaric intermediate or benzaldehyde and benzoic acid. SA can be converted into functional or non-functional metabolites such as SA-2-sulfonate, SA-Asp and MeSA, or can be stored in the vacuole as SAG, SGE, 2,3-DHBX, 2,3-DHBG, 2,5-DHBX and 2,5-DHBG. Higher SA levels induce monomerization of NPR1, translocation into the nucleus and NPR1-dependent gene expression through direct interactions with TGA transcription factors. The genes explicitly mentioned in the text are highlighted (boxed with bold line). AAO, aldehyde oxidase 4; ADH, arogenate dehydrogenase; ADT, arogenate dehydratase; AIM1, abnormal inflorescence meristem1; Asp, aspartic acid; BA2H, benzoic acid 2-hydroxylase; CM, chorismate mutase 1; DHBA, dihydroxy-benzaic acid; DHBG, dihydroxybenzoic acid glucoside; DHBX, dihydroxybenzoic acid xyloside; DLO, DMR6-like oxygenase; DMR6, SA-5 hydrolase; EDS5, enhanced disease susceptibility 5; EPS1, enhanced Pseudomonas susceptibility 1; ICS, isochorismate synthase; MES, methylesterases; NPR1, Nonexpresser of PR gene 1; PAL, phenylalanine ammonia-lyase; PBS3, avrPphB susceptible3; PDT, prephenate dehydratase; PPA-AT, plant prephenate aminotransferases; PPY-AT, phenylpyruvate aminotransferase; SA, salicylic acid; SAG, SA 2-O-β-d-glucoside; SGE, salicylate glucose ester; UGT89A2, uridine diphosphate (UDP)-glucosyltransferase.