Involvement of Arabidopsis BIG protein in cell death mediated by Myo-inositol homeostasis.
Arabidopsis
/ genetics
Arabidopsis Proteins
/ genetics
Calmodulin-Binding Proteins
/ genetics
Cluster Analysis
Epistasis, Genetic
Homeostasis
Inositol
/ metabolism
Mutation
Phenotype
Plant Growth Regulators
/ metabolism
Plant Leaves
/ metabolism
Salicylic Acid
/ metabolism
Signal Transduction
Sphingolipids
/ metabolism
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 07 2020
09 07 2020
Historique:
received:
24
09
2019
accepted:
16
03
2020
entrez:
11
7
2020
pubmed:
11
7
2020
medline:
26
1
2021
Statut:
epublish
Résumé
Programmed cell death (PCD) is essential for several aspects of plant life. We previously identified the mips1 mutant of Arabidopsis thaliana, which is deficient for the enzyme catalysing myo-inositol synthesis, and that displays light-dependent formation of lesions on leaves due to Salicylic Acid (SA) over-accumulation. Rationale of this work was to identify novel regulators of plant PCD using a genetic approach. A screen for secondary mutations that abolish the mips1 PCD phenotype identified a mutation in the BIG gene, encoding a factor of unknown molecular function that was previously shown to play pleiotropic roles in plant development and defence. Physiological analyses showed that BIG is required for lesion formation in mips1 via SA-dependant signalling. big mutations partly rescued transcriptomic and metabolomics perturbations as stress-related phytohormones homeostasis. In addition, since loss of function of the ceramide synthase LOH2 was not able to abolish cell death induction in mips1, we show that PCD induction is not fully dependent of sphingolipid accumulation as previously suggested. Our results provide further insights into the role of the BIG protein in the control of MIPS1-dependent cell death and also into the impact of sphingolipid homeostasis in this pathway.
Identifiants
pubmed: 32647331
doi: 10.1038/s41598-020-68235-4
pii: 10.1038/s41598-020-68235-4
pmc: PMC7347573
doi:
Substances chimiques
Arabidopsis Proteins
0
BIG protein, Arabidopsis
0
Calmodulin-Binding Proteins
0
Plant Growth Regulators
0
Sphingolipids
0
Inositol
4L6452S749
Salicylic Acid
O414PZ4LPZ
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11268Références
Gillaspy, G. E. The role of phosphoinositides and inositol phosphates in plant cell signaling. Adv. Exp. Med. Biol. 991, 141–157 (2013).
pubmed: 23775694
Gillaspy, G. E. The cellular language of myo-inositol signaling. New Phytol. 192, 823–839 (2011).
pubmed: 22050576
Loewus, F. A. & Murthy, P. P. N. myo-Inositol metabolism in plants. Plant Sci. 150, 1–19 (2000).
GhoshDastidar, K., Chatterjee, A., Chatterjee, A. & Majumder, A. L. Evolutionary divergence of L-myo-inositol 1-phosphate synthase: significance of a ‘core catalytic structure’. Subcell. Biochem. 39, 315–340 (2006).
pubmed: 17121281
Torabinejad, J. & Gillaspy, G. E. Functional genomics of inositol metabolism. Subcell. Biochem. 39, 47–70 (2006).
pubmed: 17121271
Meng, P. H. et al. Crosstalks between myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS ONE 4, e7364 (2009).
pubmed: 19812700
pmcid: 2754662
Donahue, J. L. et al. The Arabidopsis thaliana Myo-inositol 1-phosphate synthase1 gene is required for Myo-inositol synthesis and suppression of cell death. Plant Cell 22, 888–903 (2010).
pubmed: 20215587
pmcid: 2861443
Luo, Y. et al. D-myo-inositol-3-phosphate affects phosphatidylinositol-mediated endomembrane function in Arabidopsis and is essential for auxin-regulated embryogenesis. Plant Cell 23, 1352–1372 (2011).
pubmed: 21505066
pmcid: 3101546
Ma, L. et al. Arabidopsis FHY3 and FAR1 regulate light-induced myo-inositol biosynthesis and oxidative stress responses by transcriptional activation of MIPS1. Mol. Plant 9, 541–557 (2016).
pubmed: 26714049
Their importance in cellular organization and adaption. Michaelson, L. V, Napier, J. A., Molino, D. & Faure, J.-D. Plant sphingolipids. Biochim. Biophys. Acta 1861, 1329–1335 (2016).
Ali, U., Li, H., Wang, X. & Guo, L. Emerging roles of sphingolipid signaling in plant response to biotic and abiotic stresses. Mol. Plant 11, 1328–1343 (2018).
pubmed: 30336328
Markham, J. E. et al. Sphingolipids containing very-long-chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in arabidopsis. Plant Cell 23, 2362–2378 (2011).
pubmed: 21666002
pmcid: 3160045
Luttgeharm, K. D. et al. Overexpression of Arabidopsis ceramide synthases differentially affects growth, sphingolipid metabolism, programmed cell death, and mycotoxin resistance. Plant Physiol. 169, 1108–1117 (2015).
pubmed: 26276842
pmcid: 4587468
Zienkiewicz, A. et al. Disruption of Arabidopsis neutral ceramidases 1 and 2 results in specific sphingolipid imbalances triggering different phytohormone-dependent plant cell death programs. New Phytol. https://doi.org/10.1111/nph.16336 (2019).
doi: 10.1111/nph.16336
pubmed: 31758808
Bruggeman, Q. et al. Involvement of Arabidopsis Hexokinase1 in cell death mediated by myo-inositol accumulation. Plant Cell 27, 1801–1814 (2015).
pubmed: 26048869
pmcid: 4498202
Bruggeman, Q. et al. Chloroplast Activity And 3’phosphadenosine 5’phosphate Signaling Regulate Programmed Cell Death In ARABIDOPSIS. Plant Physiol. 170, 1745–1756 (2016).
pubmed: 26747283
pmcid: 4775142
Bruggeman, Q. et al. The polyadenylation factor subunit CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR30: a key factor of programmed cell death and a regulator of immunity in Arabidopsis. Plant Physiol. 165, 732–746 (2014).
pubmed: 24706550
pmcid: 4044851
Ruegger, M. et al. Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9, 745–757 (1997).
pubmed: 9165751
pmcid: 156953
Gil, P. et al. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985–1997 (2001).
pubmed: 11485992
pmcid: 312751
Paciorek, T. et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251–1256 (2005).
pubmed: 15988527
Kanyuka, K. et al. Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J. 35, 57–70 (2003).
pubmed: 12834402
Yamaguchi, N. et al. CRM1/BIG-mediated auxin action regulates Arabidopsis inflorescence development. Plant Cell Physiol. 48, 1275–1290 (2007).
pubmed: 17652113
Yamaguchi, N. & Komeda, Y. The role of CORYMBOSA1/BIG and auxin in the growth of Arabidopsis pedicel and internode. Plant Sci. 209, 64–74 (2013).
pubmed: 23759104
Ivanova, A. et al. A Functional antagonistic relationship between auxin and mitochondrial retrograde signaling regulates alternative oxidase1a expression in Arabidopsis. Plant Physiol. 165, 1233–1254 (2014).
pubmed: 24820025
pmcid: 4081334
Hearn, T. J. et al. BIG regulates dynamic adjustment of circadian period in Arabidopsis thaliana. Plant Physiol. https://doi.org/10.1104/pp.18.00571 (2018).
doi: 10.1104/pp.18.00571
pubmed: 29997180
pmcid: 6130016
He, J. et al. The BIG protein distinguishes the process of CO2 -induced stomatal closure from the inhibition of stomatal opening by CO2. New Phytol. 218, 232–241 (2018).
pubmed: 29292834
pmcid: 5887946
Zhang, R.-X. et al. BIG regulates stomatal immunity and jasmonate production in Arabidopsis. New Phytol. 222, 335–348 (2019).
pubmed: 30372534
Simon, C. et al. The differential spatial distribution of secondary metabolites in Arabidopsis leaves reacting hypersensitively to Pseudomonas syringae pv. tomato is dependent on the oxidative burst. J. Exp. Bot. 61, 3355–3370 (2010).
pubmed: 20530195
Chen, H. & Xiong, L. myo-Inositol-1-phosphate synthase is required for polar auxin transport and organ development. J. Biol. Chem. 285, 24238–24247 (2010).
pubmed: 20516080
pmcid: 2911297
Chang, Y.-F., Imam, J. S. & Wilkinson, M. F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51–74 (2007).
pubmed: 17352659
Du, Z., Zhou, X., Ling, Y., Zhang, Z. & Su, Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-70 (2010).
pubmed: 20435677
pmcid: 2896167
Guo, X., Lu, W., Ma, Y., Qin, Q. & Hou, S. The BIG gene is required for auxin-mediated organ growth in Arabidopsis. Planta 237, 1135–1147 (2013).
pubmed: 23288076
Luttgeharm, K. D., Kimberlin, A. N. & Cahoon, E. B. Plant Sphingolipid Metabolism and Function. Subcell. Biochem. 86, 249–286 (2016).
pubmed: 27023239
Markham, J. E., Li, J., Cahoon, E. B. & Jaworski, J. G. Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 281, 22684–22694 (2006).
pubmed: 16772288
Chaouch, S. & Noctor, G. Myo-inositol abolishes salicylic acid-dependent cell death and pathogen defence responses triggered by peroxisomal hydrogen peroxide. New Phytol. 188, 711–718 (2010).
pubmed: 20807338
Meteignier, L.-V. et al. Translatome analysis of an NB-LRR immune response identifies important contributors to plant immunity in Arabidopsis. J. Exp. Bot. 68, 2333–2344 (2017).
pubmed: 28369573
Qi, L. et al. Arabidopsis thaliana plants differentially modulate auxin biosynthesis and transport during defense responses to the necrotrophic pathogen Alternaria brassicicola. New Phytol. 195, 872–882 (2012).
pubmed: 22731664
Sun, J. et al. Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21, 1495–1511 (2009).
pubmed: 19435934
pmcid: 2700526
Hong, J. H. et al. A sacrifice-for-survival mechanism protects root stem cell niche from chilling stress. Cell 170, 102-113.e14 (2017).
pubmed: 28648662
Gawronski, P. et al. Mitogen-activated protein kinase 4 is a salicylic acid-independent regulator of growth but not of photosynthesis in Arabidopsis. Mol. Plant 7, 1151–1166 (2014).
pubmed: 24874867
König, S. et al. Arabidopsis mutants of sphingolipid fatty acid α-hydroxylases accumulate ceramides and salicylates. New Phytol. 196, 1086–1097 (2012).
pubmed: 23025549
Samson, F. et al. FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res. 30, 94–97 (2002).
pubmed: 11752264
pmcid: 99145
Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657 (2003).
pubmed: 12893945
pmcid: 12893945
Pacurar, D. I. et al. A collection of INDEL markers for map-based cloning in seven Arabidopsis accessions. J. Exp. Bot. 63, 2491–2501 (2012).
pubmed: 22282537
pmcid: 3346218
Latrasse, D. et al. The quest for epigenetic regulation underlying unisexual flower development in Cucumis melo. Epigenet. Chromatin 10, 22 (2017).
Le Roux, C. et al. The hnRNP-Q protein LIF2 participates in the plant immune response. PLoS ONE 9, e99343 (2014).
pubmed: 24914891
pmcid: 4051675
Tellier, F., Maia-Grondard, A., Schmitz-Afonso, I. & Faure, J.-D. Comparative plant sphingolipidomic reveals specific lipids in seeds and oil. Phytochemistry 103, 50–58 (2014).
pubmed: 24731258