Direct inhibition of phosphate transport by immune signaling in Arabidopsis

拟南芥 生物 磷酸盐 生物化学 信号转导 免疫系统 细胞生物学 遗传学 突变体 基因
作者
Julian Dindas,Thomas A. DeFalco,Gang Yu,Lu Zhang,Pascale David,Marta Bjornson,Marie‐Christine Thibaud,Valéria Custódio,Gabriel Castrillo,Laurent Nussaume,Alberto P. Macho,Cyril Zipfel
出处
期刊:Current Biology [Elsevier BV]
卷期号:32 (2): 488-495.e5 被引量:38
标识
DOI:10.1016/j.cub.2021.11.063
摘要

Soil availability of inorganic ortho-phosphate (PO43−, Pi) is a key determinant of plant growth and fitness.1Bieleski R.L. Phosphate pools, phosphate transport, and phosphate availability.Annu. Rev. Plant Physiol. 1973; 24: 225-252Crossref Google Scholar Plants regulate the capacity of their roots to take up inorganic phosphate by adapting the abundance of H+-coupled phosphate transporters of the PHOSPHATE TRANSPORTER 1 (PHT1) family2Nussaume L. Kanno S. Javot H. Marin E. Pochon N. Ayadi A. Nakanishi T.M. Thibaud M.C. Phosphate import in plants: focus on the PHT1 transporters.Front. Plant Sci. 2011; 2: 83Crossref PubMed Scopus (305) Google Scholar at the plasma membrane (PM) through transcriptional and post-translational changes driven by the genetic network of the phosphate starvation response (PSR).3Shin H. Shin H.-S. Dewbre G.R. Harrison M.J. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments.Plant J. 2004; 39: 629-642Crossref PubMed Scopus (525) Google Scholar, 4Misson J. Thibaud M.C. Bechtold N. Raghothama K. Nussaume L. Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants.Plant Mol. Biol. 2004; 55: 727-741Crossref PubMed Scopus (183) Google Scholar, 5Thibaud M.C. Arrighi J.F. Bayle V. Chiarenza S. Creff A. Bustos R. Paz-Ares J. Poirier Y. Nussaume L. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis.Plant J. 2010; 64: 775-789Crossref PubMed Scopus (204) Google Scholar, 6Bayle V. Arrighi J.-F.F. Creff A. Nespoulous C. Vialaret J. Rossignol M. Gonzalez E. Paz-Ares J. Nussaume L. Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation.Plant Cell. 2011; 23: 1523-1535Crossref PubMed Scopus (164) Google Scholar, 7Park B.S. Seo J.S. Chua N.H. NITROGEN LIMITATION ADAPTATION recruits PHOSPHATE2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis.Plant Cell. 2014; 26: 454-464Crossref PubMed Scopus (158) Google Scholar, 8Liao Y.Y. Li J.L. Pan R.L. Chiou T.J. Structure-function analysis reveals amino acid residues of Arabidopsis phosphate transporter AtPHT1;1 crucial for its activity.Front. Plant Sci. 2019; 10: 1158Crossref PubMed Scopus (7) Google Scholar Increasing evidence also shows that plants integrate immune responses to alleviate phosphate starvation stress through the association with beneficial microbes.9Castrillo G. Teixeira P.J.P.L. Paredes S.H. Law T.F.T.F. de Lorenzo L. Feltcher M.E. Finkel O.M. Breakfield N.W. Mieczkowski P. Jones C.D. et al.Root microbiota drive direct integration of phosphate stress and immunity.Nature. 2017; 543: 513-518Crossref PubMed Scopus (354) Google Scholar, 10Finkel O.M. Salas-González I. Castrillo G. Spaepen S. Law T.F. Teixeira P.J.P.L. Jones C.D. Dangl J.L. The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response.PLoS Biol. 2019; 17: e3000534Crossref PubMed Scopus (58) Google Scholar, 11Shi J. Zhao B. Zheng S. Zhang X. Wang X. Dong W. Xie Q. Wang G. Xiao Y. Chen F. et al.A phosphate starvation response-centered network regulates mycorrhizal symbiosis.Cell. 2021; 184: 5527-5540.e18Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar Whether and how such phosphate transport is regulated upon activation of immune responses is yet uncharacterized. To address this question, we first developed quantitative assays based on changes in the electrical PM potential to measure active Pi transport in roots in real time. By inserting micro-electrodes into bulging root hairs, we were able to determine key characteristics of phosphate transport in intact Arabidopsis thaliana (hereafter Arabidopsis) seedlings. The fast Pi-induced depolarization observed was dependent on the activity of the major phosphate transporter PHT1;4. Notably, we observed that this PHT1;4-mediated phosphate uptake is repressed upon activation of pattern-triggered immunity. This inhibition depended on the receptor-like cytoplasmic kinases BOTRYTIS-INDUCED KINASE 1 (BIK1) and PBS1-LIKE KINASE 1 (PBL1), which both phosphorylated PHT1;4. As a corollary to this negative regulation of phosphate transport by immune signaling, we found that PHT1;4-mediated phosphate uptake normally negatively regulates anti-bacterial immunity in roots. Collectively, our results reveal a mechanism linking plant immunity and phosphate homeostasis, with BIK1/PBL1 providing a molecular integration point between these two important pathways.
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