Terrile, M.C.; París, R.; Calderón Villalobos, L.I.; Iglesias, M.J.; Lamattina, L.; Estelle, M.; Casalongué, C.A. Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70, 492-500, (2012) DOI: 10.1111/j.1365-313X.2011.04885.x
Previous studies have demonstrated that auxin (indole-3-acetic acid) and nitric oxide (NO) are plant growth regulators that coordinate several plant physiological responses determining root architecture. Nonetheless, the way in which these factors interact to affect these growth and developmental processes is not well understood. The Arabidopsis thaliana F-box proteins TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX (TIR1/AFB) are auxin receptors that mediate degradation of AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) repressors to induce auxin-regulated responses. A broad spectrum of NO-mediated protein modifications are known in eukaryotic cells. Here, we provide evidence that NO donors increase auxin-dependent gene expression while NO depletion blocks Aux/IAA protein degradation. NO also enhances TIR1-Aux/IAA interaction as evidenced by pull-down and two-hybrid assays. In addition, we provide evidence for NO-mediated modulation of auxin signaling through S-nitrosylation of the TIR1 auxin receptor. S-nitrosylation of cysteine is a redox-based post-translational modification that contributes to the complexity of the cellular proteome. We show that TIR1 C140 is a critical residue for TIR1Aux/IAA interaction and TIR1 function. These results suggest that TIR1 S-nitrosylation enhances TIR1Aux/IAA interaction, facilitating Aux/IAA degradation and subsequently promoting activation of gene expression. Our findings underline the importance of NO in phytohormone signaling pathways.
Goetz, S.; Hellwege, A.; Stenzel, I.; Kutter, C.; Hauptmann, V.; Forner, S.; McCaig, B.; Hause, G.; Miersch, O.; Wasternack, C.; Hause, B. Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol 158, 1715-1727, (2012) DOI: 10.1104/pp.111.192658
Oxylipins including jasmonates are signaling compounds in plant growth, development, and responses to biotic and abiotic stresses. In Arabidopsis (Arabidopsis thaliana) most mutants affected in jasmonic acid (JA) biosynthesis and signaling are male sterile, whereas the JA-insensitive tomato (Solanum lycopersicum) mutant jai1 is female sterile. The diminished seed formation in jai1 together with the ovule-specific accumulation of the JA biosynthesis enzyme allene oxide cyclase (AOC), which correlates with elevated levels of JAs, suggest a role of oxylipins in tomato flower/seed development. Here, we show that 35S::SlAOC-RNAi lines with strongly reduced AOC in ovules exhibited reduced seed set similarly to the jai1 plants. Investigation of embryo development of wild-type tomato plants showed preferential occurrence of AOC promoter activity and AOC protein accumulation in the developing seed coat and the embryo, whereas 12-oxo-phytodienoic acid (OPDA) was the dominant oxylipin occurring nearly exclusively in the seed coat tissues. The OPDA- and JA-deficient mutant spr2 was delayed in embryo development and showed an increased programmed cell death in the developing seed coat and endosperm. In contrast, the mutant acx1a, which accumulates preferentially OPDA and residual amount of JA, developed embryos similar to the wild type, suggesting a role of OPDA in embryo development. Activity of the residual amount of JA in the acx1a mutant is highly improbable since the known reproductive phenotype of the JA-insensitive mutant jai1 could be rescued by wound-induced formation of OPDA. These data suggest a role of OPDA or an OPDA-related compound for proper embryo development possibly by regulating carbohydrate supply and detoxification.
Stenzel, I.; Otto, M.; Delker, C.; Kirmse, N.; Schmidt, D.; Miersch, O.; Hause, B.; Wasternack, C. ALLENE OXIDE CYCLASE (AOC) gene family members of
Arabidopsis thaliana: tissue- and organ-specific promoter activities and
in vivo heteromerization J Exp Bot 63, 6125-6138, (2012) DOI: 10.1093/jxb/ers261
Jasmonates are important signals in plant stress responses and plant development. An essential step in the biosynthesis of jasmonic acid (JA) is catalysed by ALLENE OXIDE CYCLASE (AOC) which establishes the naturally occurring enantiomeric structure of jasmonates. In Arabidopsis thaliana, four genes encode four functional AOC polypeptides (AOC1, AOC2, AOC3, and AOC4) raising the question of functional redundancy or diversification. Analysis of transcript accumulation revealed an organ-specific expression pattern, whereas detailed inspection of transgenic lines expressing the GUS reporter gene under the control of individual AOC promoters showed partially redundant promoter activities during development: (i) In fully developed leaves, promoter activities of AOC1, AOC2, and AOC3 appeared throughout all leaf tissue, but AOC4 promoter activity was vascular bundle-specific; (ii) only AOC3 and AOC4 showed promoter activities in roots; and (iii) partially specific promoter activities were found for AOC1 and AOC4 in flower development. In situ hybridization of flower stalks confirmed the GUS activity data. Characterization of single and double AOC loss-of-function mutants further corroborates the hypothesis of functional redundancies among individual AOCs due to a lack of phenotypes indicative of JA deficiency (e.g. male sterility). To elucidate whether redundant AOC expression might contribute to regulation on AOC activity level, protein interaction studies using bimolecular fluorescence complementation (BiFC) were performed and showed that all AOCs can interact among each other. The data suggest a putative regulatory mechanism of temporal and spatial fine-tuning in JA formation by differential expression and via possible heteromerization of the four AOCs.
Brandt, R.; Salla-Martret, M.; Bou-Torrent, J.; Musielak, T.; Stahl, M.; Lanz, C.; Ott, F.; Schmid, M.; Greb, T.; Schwarz, M.; Choi, S.-B.; Barton, M. K.; Reinhart, B. J.; Liu, T.; Quint, M.; Palauqui, J.-C.; Martínez-García, J. F.; Wenkel, S. Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses Plant J 72, 31-42, (2012) DOI: 10.1111/j.1365-313X.2012.05049.x
Unlike the situation in animals, the final morphology of the plant body is highly modulated by the environment. During Arabidopsis development, intrinsic factors provide the framework for basic patterning processes. CLASS III HOMEODOMAIN LEUCINE ZIPPER (HD-ZIPIII) transcription factors are involved in embryo, shoot and root patterning. During vegetative growth HD-ZIPIII proteins control several polarity set-up processes such as in leaves and the vascular system. We have identified several direct target genes of the HD-ZIPIII transcription factor REVOLUTA (REV) using a chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) approach. This analysis revealed that REV acts upstream of auxin biosynthesis and affects directly the expression of several class II HD-ZIP transcription factors that have been shown to act in the shade-avoidance response pathway. We show that, as well as involvement in basic patterning, HD-ZIPIII transcription factors have a critical role in the control of the elongation growth that is induced when plants experience shade. Leaf polarity is established by the opposed actions of HD-ZIPIII and KANADI transcription factors. Finally, our study reveals that the module that consists of HD-ZIPIII/KANADI transcription factors controls shade growth antagonistically and that this antagonism is manifested in the opposed regulation of shared target genes.
Wasternack, C.; Goetz, S.; Hellwege, A.; Forner, S.; Strnad, M.; Hause, B. Another JA/COI1-independent role of OPDA detected in tomato embryo development. Plant Signal Behav 7, 1349-1353, (2012) DOI: 10.4161/psb.21551
Jasmonates (JAs) are ubiquitously occurring signaling compounds in plants formed in response to biotic and abiotic stress as well as in development. (+)-7-iso-jasmonoyl isoleucine, the bioactive JA, is involved in most JA-dependent processes mediated by the F-box protein COI1 in a proteasome-dependent manner. However, there is an increasing number of examples, where the precursor of JA biosynthesis, cis-(+)-12-oxophytodienoic acid (OPDA) is active in a JA/COI1-independent manner. Here, we discuss those OPDA-dependent processes, thereby giving emphasis on tomato embryo development. Recent data on seed coat-generated OPDA and its role in embryo development is discussed based on biochemical and genetic evidences.
Antolín-Llovera, M.; Ried, M. K.; Binder, A.; Parniske, M. Receptor Kinase Signaling Pathways in Plant-Microbe Interactions Annu Rev Phytopathol 50, 451-473, (2012) DOI: 10.1146/annurev-phyto-081211-173002
Plant receptor-like kinases (RLKs) function in diverse signaling
pathways, including the responses to microbial signals in symbiosis and
defense. This versatility is achieved with a common overall structure:
an extracytoplasmic domain (ectodomain) and an intracellular protein
kinase domain involved in downstream signal transduction. Various
surfaces of the leucine-rich repeat (LRR) ectodomain superstructure are
utilized for interaction with the cognate ligand in both plant and
animal receptors. RLKs with lysin-motif (LysM) ectodomains confer
recognitional specificity toward N-acetylglucosamine-containing
signaling molecules, such as chitin, peptidoglycan (PGN), and rhizobial
nodulation factor (NF), that induce immune or symbiotic responses.
Signaling downstream of RLKs does not follow a single pattern; instead,
the detailed analysis of brassinosteroid (BR) signaling, innate
immunity, and symbiosis revealed at least three largely nonoverlapping
pathways. In this review, we focus on RLKs involved in plant-microbe
interactions and contrast the signaling pathways leading to symbiosis
Den Herder, G.; Yoshida, S.; Antolín-Llovera, M.; Ried, M. K.; Parniske, M. Lotus japonicus E3 Ligase SEVEN IN ABSENTIA4
Destabilizes the Symbiosis Receptor-Like Kinase SYMRK and Negatively
Regulates Rhizobial Infection Plant Cell 24, 1691-1707, (2012) DOI: 10.1105/tpc.110.082248
The Lotus japonicus SYMBIOSIS RECEPTOR-LIKE KINASE (SYMRK) is required
for symbiotic signal transduction upon stimulation of root cells by
microbial signaling molecules. Here, we identified members of the SEVEN
IN ABSENTIA (SINA) E3 ubiquitin-ligase family as SYMRK interactors and
confirmed their predicted ubiquitin-ligase activity. In Nicotiana
benthamiana leaves, SYMRK–yellow fluorescent protein was localized at
the plasma membrane, and interaction with SINAs, as determined by
bimolecular fluorescence complementation, was observed in small punctae
at the cytosolic interface of the plasma membrane. Moreover,
fluorescence-tagged SINA4 partially colocalized with SYMRK and caused
SYMRK relocalization as well as disappearance of SYMRK from the plasma
membrane. Neither the localization nor the abundance of Nod-factor
receptor1 was altered by the presence of SINA4. SINA4 was
transcriptionally upregulated during root symbiosis, and rhizobia
inoculated roots ectopically expressing SINA4 showed reduced SYMRK
protein levels. In accordance with a negative regulatory role in
symbiosis, infection thread development was impaired upon ectopic
expression of SINA4. Our results implicate SINA4 E3 ubiquitin ligase in
the turnover of SYMRK and provide a conceptual mechanism for its
symbiosis-appropriate spatio-temporal containment.