Skip to main content
Log in

Modulation of plant immunity and biotic interactions under phosphate deficiency

  • JPR Symposium
  • Update of Phosphate Transport Regulations
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Phosphorus (P) is an essential macronutrient for plant life and growth. P is primarily acquired in the form of inorganic phosphate (Pi) from soil. To cope with Pi deficiency, plants have evolved an elaborate system to improve Pi acquisition and utilization through an array of developmental and physiological changes, termed Pi starvation response (PSR). Plants also assemble and manage mutualistic microbes to enhance Pi uptake, through integrating PSR and immunity signaling. A trade-off between plant growth and defense favors the notion that plants lower a cellular state of immunity to accommodate host-beneficial microbes for nutrition and growth at the cost of infection risk. However, the existing data indicate that plants selectively activate defense responses against pathogens, but do not or less against non-pathogens, even under nutrient deficiency. In this review, we highlight recent advances in the principles and mechanisms with which plants balance immunity and growth-related processes to optimize their adaptation to Pi deficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abel S (2017) Phosphate scouting by root tips. Curr Opin Plant Biol 39:168–177

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Matsuoka H, Hayashi H (2002) Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol Plant Microbe Interact 15:334–340

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    Article  CAS  PubMed  Google Scholar 

  • Aleksza D, Horváth GV, Sándor G, Szabados L (2017) Proline accumulation is regulated by transcription factors associated with phosphate starvation. Plant Physiol 175:555–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakshi M, Vahabi K, Bhattacharya S, Sherameti I, Varma A, Yeh K-W, Baldwin I, Johri AK, Oelmüller R (2015) WRKY6 restricts Piriformospora indica-stimulated and phosphate-induced root development in Arabidopsis. BMC Plant Biol 15:305

    Article  PubMed  PubMed Central  Google Scholar 

  • Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C, Teulon J-M, Creff A, Bissler M, Brouchoud C, Hagège A et al (2017) Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun 8:15300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barragán-Rosillo AC, Peralta-Alvarez CA, Ojeda-Rivera JO, Arzate-Mejía RG, Recillas-Targa F, Herrera-Estrella L (2021) Genome accessibility dynamics in response to phosphate limitation is controlled by the PHR1 family of transcription factors in Arabidopsis. Proc Natl Acad Sci U S A 118:e2107558118

  • Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bian C, Demirer GS, Brady SM (2022) GLRs: mediating a defense-regeneration tradeoff in plants. Dev Cell 57:417–418

    Article  CAS  PubMed  Google Scholar 

  • Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E et al (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017

    Article  CAS  PubMed  Google Scholar 

  • Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:e1001102

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai J, Jiang Y, Ritchie ES, Macho AP, Yu F, Wu D (2023) Manipulation of plant metabolism by pathogen effectors: more than just food. FEMS Microbiol Rev 47:fuad007

    Article  CAS  PubMed  Google Scholar 

  • Campos-Soriano L, Bundó M, Bach-Pages M, Chiang S-F, Chiou T-J, San Segundo B (2020) Phosphate excess increases susceptibility to pathogen infection in rice. Mol Plant Pathol 21:555–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castel B, El Mahboubi K, Jacquet C, Delaux P-M (2024) Immunobiodiversity: conserved and specific immunity across land plants and beyond. Mol Plant 17:92–111

    Article  CAS  PubMed  Google Scholar 

  • Castrillo G, Teixeira PJPL, Paredes SH, Law TF, de Lorenzo L, Feltcher ME, Finkel OM, Breakfield NW, Mieczkowski P, Jones CD et al (2017) Root microbiota drive direct integration of phosphate stress and immunity. Nature 543:513–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan C, Liao Y-Y, Chiou T-J (2021) The impact of phosphorus on plant immunity. Plant Cell Physiol 62:582–589

    Article  CAS  PubMed  Google Scholar 

  • Chen A, Gu M, Sun S, Zhu L, Hong S, Xu G (2011) Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol 189:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Ni L, Chen J, Sun M, Qin C, Zhang G, Zhang A, Jiang M (2021) Rice calcium/calmodulin-dependent protein kinase directly phosphorylates a mitogen-activated protein kinase kinase to regulate abscisic acid responses. Plant Cell 33:1790–1812

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng YT, Zhang L, He SY (2019) Plant-microbe interactions facing environmental challenge. Cell Host Microbe 26:183–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevalier F, Cuyas L, Jouhet J, Gros VR, Chiarenza S, Secco D, Whelan J, Seddiki K, Block MA, Nussaume L et al (2019) Interplay between jasmonic acid, phosphate signaling and the regulation of glycerolipid homeostasis in Arabidopsis. Plant Cell Physiol 60:1260–1273

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science 343:290–294

    Article  CAS  PubMed  Google Scholar 

  • Colaianni NR, Parys K, Lee H-S, Conway JM, Kim NH, Edelbacher N, Mucyn TS, Madalinski M, Law TF, Jones CD et al (2021) A complex immune response to flagellin epitope variation in commensal communities. Cell Host Microbe 29:635-649.e9

    Article  CAS  PubMed  Google Scholar 

  • Crombez H, Motte H, Beeckman T (2019) Tackling plant phosphate starvation by the roots. Dev Cell 48:599–615

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci U S A 103:6765–6770

  • Das D, Paries M, Hobecker K, Gigl M, Dawid C, Lam H-M, Zhang J, Chen M, Gutjahr C (2022) Phosphate starvation response transcription factors enable arbuscular mycorrhiza symbiosis. Nat Commun 13:477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Díaz-González S, Marín P, Sánchez R, Arribas C, Kruse J, González-Melendi P, Brunner F, Sacristán S (2020) Mutualistic fungal endophyte Colletotrichum tofieldiae Ct0861 colonizes and increases growth and yield of maize and tomato plants. Agronomy 10:1493

    Article  Google Scholar 

  • Dindas J, DeFalco TA, Yu G, Zhang L, David P, Bjornson M, Thibaud M-C, Custódio V, Castrillo G, Nussaume L et al (2022) Direct inhibition of phosphate transport by immune signaling in Arabidopsis. Curr Biol 32:488-495.e5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong J, Ma G, Sui L, Wei M, Satheesh V, Zhang R, Ge S, Li J, Zhang T-E, Wittwer C et al (2019a) Inositol pyrophosphate InsP8 acts as an intracellular phosphate signal in Arabidopsis. Mol Plant 12:1463–1473

    Article  CAS  PubMed  Google Scholar 

  • Dong Z, Li W, Liu J, Li L, Pan S, Liu S, Gao J, Liu L, Liu X, Wang G-L et al (2019b) The rice phosphate transporter protein OsPT8 regulates disease resistance and plant growth. Sci Rep 9:5408

    Article  PubMed  PubMed Central  Google Scholar 

  • Drew GC, Stevens EJ, King KC (2021) Microbial evolution and transitions along the parasite-mutualist continuum. Nat Rev Microbiol 19:623–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du Z, Deng S, Wu Z, Cai H, Xu F, Shi L, Wang S, Ding G, Wang C (2022) Characterization of the PHOSPHATE RESPONSE 2-dependent and -independent Pi-starvation response secretome in rice. J Exp Bot 73:6955–6970

    Article  CAS  PubMed  Google Scholar 

  • Entila F, Han X, Mine A, Schulze-Lefert P, Tsuda K (2024) Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS. Nat Commun 15:456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkel OM, Salas-González I, Castrillo G, Spaepen S, Law TF, Teixeira PJPL, Jones CD, Dangl JL (2019) The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLoS Biol 17:e3000534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frerigmann H, Piotrowski M, Lemke R, Bednarek P, Schulze-Lefert P (2021) A Network of phosphate starvation and immune-related signaling and metabolic pathways controls the interaction between Arabidopsis thaliana and the beneficial fungus Colletotrichum tofieldiae. Mol Plant Microbe Interact 34:560–570

    Article  CAS  PubMed  Google Scholar 

  • Garrido-Oter R, Nakano RT, Dombrowski N, Ma K-W, AgBiome Team, McHardy AC, Schulze-Lefert P (2018) Modular traits of the Rhizobiales root microbiota and their evolutionary relationship with symbiotic Rhizobia. Cell Host Microbe 24:155-167.e5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan Z, Zhang Q, Zhang Z, Zuo J, Chen J, Liu R, Savarin J, Broger L, Cheng P, Wang Q et al (2022) Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2 – PHR2 complex. Nat Commun 13:1581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gulabani H, Goswami K, Walia Y, Roy A, Noor JJ, Ingole KD, Kasera M, Laha D, Giehl RFH, Schaaf G et al (2022) Arabidopsis inositol polyphosphate kinases IPK1 and ITPK1 modulate crosstalk between SA-dependent immunity and phosphate-starvation responses. Plant Cell Rep 41:347–363

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Alanís D, Yong-Villalobos L, Jiménez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A, Mora-Macías J, Sánchez-Rodríguez F, Cruz-Ramírez A, Herrera-Estrella L (2017) Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev Cell 41:555-570.e3

    Article  PubMed  Google Scholar 

  • Hacquard S, Kracher B, Hiruma K, Münch PC, Garrido-Oter R, Thon MR, Weimann A, Damm U, Dallery J-F, Hainaut M et al (2016) Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat Commun 7:11362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hacquard S, Spaepen S, Garrido-Oter R, Schulze-Lefert P (2017) Interplay between innate immunity and the plant microbiota. Annu Rev Phytopathol 55:565–589

    Article  CAS  PubMed  Google Scholar 

  • Han X, Tsuda K (2022) Evolutionary footprint of plant immunity. Curr Opin Plant Biol 67:102209

    Article  PubMed  Google Scholar 

  • Haney CH, Samuel BS, Bush J, Ausubel FM (2015) Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat Plants 1:15051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He K, Du J, Han X, Li H, Kui M, Zhang J, Huang Z, Fu Q, Jiang Y, Hu Y (2023) Phosphate starvation response1 (PHR1) interacts with Jasmonate Zim-domain (JAZ) and MYC2 to modulate phosphate deficiency-induced jasmonate signaling in Arabidopsis. Plant Cell 35:2132–2156

    Article  PubMed  PubMed Central  Google Scholar 

  • Hepper CM (1983) The effect of nitrate and phosphate on the vesicular-arbuscular mycorrhizal infection of lettuce. New Phytol 93:389–399

    Article  CAS  Google Scholar 

  • Hiruma K, Aoki S, Takino J, Higa T, Utami YD, Shiina A, Okamoto M, Nakamura M, Kawamura N, Ohmori Y et al (2023) A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae. Nat Commun 14:5288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ et al (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Soil Res 35:227

    Article  CAS  Google Scholar 

  • Hou S, Tsuda K (2022) Salicylic acid and jasmonic acid crosstalk in plant immunity. Essays Biochem 66:647–656

    Article  CAS  PubMed  Google Scholar 

  • Huang T-K, Han C-L, Lin S-I, Chen Y-J, Tsai Y-C, Chen Y-R, Chen J-W, Lin W-Y, Chen P-M, Liu T-Y et al (2013) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots[W][Open]. Plant Cell 25:4044–4060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isidra-Arellano MC, Delaux P-M, Valdés-López O (2021) The phosphate starvation response system: its role in the regulation of plant–microbe interactions. Plant Cell Physiol 62:392–400

    Article  CAS  PubMed  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104:1720–1725

  • Jia X, Wang L, Nussaume L, Yi K (2023) Cracking the code of plant central phosphate signaling. Trends Plant Sci 28:267–270

    Article  CAS  PubMed  Google Scholar 

  • Jian Y, Gong D, Wang Z, Liu L, He J, Han X, Tsuda K (2024) How plants manage pathogen infection. EMBO Rep 25:31–44

    Article  PubMed  Google Scholar 

  • Johri AK, Oelmüller R, Dua M, Yadav V, Kumar M, Tuteja N, Varma A, Bonfante P, Persson BL, Stroud RM (2015) Fungal association and utilization of phosphate by plants: success, limitations, and future prospects. Front Microbiol 6:984

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Khan GA, Vogiatzaki E, Glauser G, Poirier Y (2016) Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory. Plant Physiol 171:632–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobae Y, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Zhang C, Zheng H, Sun M, Zhang F, Zhang M, Cui F, Lv D, Liu L, Guo S et al (2020) Antagonistic interaction between auxin and SA signaling pathways regulates bacterial infection through lateral root in Arabidopsis. Cell Rep 32:108060

    Article  CAS  PubMed  Google Scholar 

  • Kong Y, Wang G, Chen X, Li L, Zhang X, Chen S, He Y, Hong G (2021) OsPHR2 modulates phosphate starvation-induced OsMYC2 signalling and resistance to Xanthomonas oryzae pv. oryzae. Plant Cell Environ 44:3432–3444

    Article  CAS  PubMed  Google Scholar 

  • Lanfranco L, Fiorilli V, Venice F, Bonfante P (2018) Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J Exp Bot 69:2175–2188

    Article  CAS  PubMed  Google Scholar 

  • Lei L, Li Y, Wang Q, Xu J, Chen Y, Yang H, Ren D (2014) Activation of MKK9-MPK3/MPK6 enhances phosphate acquisition in Arabidopsis thaliana. New Phytol 203:1146–1160

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J, Choi J, Kang Ch, Qiu J, Stacey G (2013) Nonlegumes respond to rhizobial nod factors by suppressing the innate immune response. Science 341:1384–1387

    Article  CAS  PubMed  Google Scholar 

  • Lin W-Y, Huang T-K, Chiou T-J (2013) Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane–localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25:4061–4074

  • Liu C, Jiang M, Yuan MM, Wang E, Bai Y, Crowther TW, Zhou J, Ma Z, Zhang L, Wang Y et al (2023a) Root microbiota confers rice resistance to aluminium toxicity and phosphorus deficiency in acidic soils. Nat Food 4:912–924

    Article  CAS  PubMed  Google Scholar 

  • Liu T-Y, Huang T-K, Tseng C-Y, Lai Y-S, Lin S-I, Lin W-Y, Chen J-W, Chiou T-J (2012) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24:2168–2183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wilson AJ, Han J, Hui A, O’Sullivan L, Huan T, Haney CH (2023) Amino acid availability determines plant immune homeostasis in the rhizosphere microbiome. mBio 14:e0342422

    Article  PubMed  Google Scholar 

  • Liu Z, Wu X, Wang E, Liu Y, Wang Y, Zheng Q, Han Y, Chen Z, Zhang Y (2022) PHR1 positively regulates phosphate starvation-induced anthocyanin accumulation through direct upregulation of genes F3’H and LDOX in Arabidopsis. Planta 256:42

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Tsuda K (2021) Intimate association of PRR- and NLR-mediated signaling in plant immunity. Mol Plant Microbe Interact 34:3–14

    Article  PubMed  Google Scholar 

  • Lu Y-T, Li M-Y, Cheng K-T, Tan CM, Su L-W, Lin W-Y, Shih H-T, Chiou T-J, Yang J-Y (2014) Transgenic plants that express the phytoplasma effector SAP11 show altered phosphate starvation and defense responses. Plant Physiol 164:1456–1469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma K-W, Niu Y, Jia Y, Ordon J, Copeland C, Emonet A, Geldner N, Guan R, Stolze SC, Nakagami H et al (2021) Coordination of microbe–host homeostasis by crosstalk with plant innate immunity. Nat Plants 7:814–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Walker RK, Zhao Y, Berkowitz GA (2012) Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. Proc Natl Acad Sci U S A 109:19852–19857

  • Matthus E, Wilkins KA, Mohammad-Sidik A, Ning Y, Davies JM (2022) Spatial origin of the extracellular ATP-induced cytosolic calcium signature in Arabidopsis thaliana roots: wave formation and variation with phosphate nutrition. Plant Biol 24:863–873

    Article  CAS  PubMed  Google Scholar 

  • McCombe CL, Wegner A, Zamora CS, Casanova F, Aditya S, Greenwood JR, Wirtz L, Paula S de, England E, Shang S, et al (2023) Plant pathogenic fungi hijack phosphate starvation signaling with conserved enzymatic effectors. 2023.11.14.566975. https://doi.org/10.1101/2023.11.14.566975. [PREPRINT]

  • Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González J, Jiménez-Domínguez G, Chávez-Calvillo G, Rellán-Álvarez R, Herrera-Estrella L (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci U S A 114:E3563–E3572

  • Morcillo RJ, Singh SK, He D, An G, Vílchez JI, Tang K, Yuan F, Sun Y, Shao C, Zhang S et al (2020) Rhizobacterium-derived diacetyl modulates plant immunity in a phosphate-dependent manner. EMBO J 39:e102602

    Article  CAS  PubMed  Google Scholar 

  • Motte H, Beeckman T (2017) PHR1 balances between nutrition and immunity in plants. Dev Cell 41:5–7

    Article  CAS  PubMed  Google Scholar 

  • Müller J, Toev T, Heisters M, Teller J, Moore KL, Hause G, Dinesh DC, Bürstenbinder K, Abel S (2015) Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell 33:216–230

    Article  PubMed  Google Scholar 

  • Müller LM, Flokova K, Schnabel E, Sun X, Fei Z, Frugoli J, Bouwmeester HJ, Harrison MJ (2019) A CLE-SUNN module regulates strigolactone content and fungal colonization in arbuscular mycorrhiza. Nat Plants 5:933–939

    Article  PubMed  Google Scholar 

  • Nagatoshi Y, Ikazaki K, Kobayashi Y, Mizuno N, Sugita R, Takebayashi Y, Kojima M, Sakakibara H, Kobayashi NI, Tanoi K et al (2023) Phosphate starvation response precedes abscisic acid response under progressive mild drought in plants. Nat Commun 14:5047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura Y (2013) Phosphate starvation and membrane lipid remodeling in seed plants. Progress Lipid Res 52:43–50

    Article  CAS  Google Scholar 

  • Nakano RT, Shimasaki T (2024) Long-term consequences of PTI activation and its manipulation by root-associated microbiota. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcae033

  • Ngou BPM, Ahn H-K, Ding P, Jones JDG (2021) Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592:110–115

    Article  CAS  PubMed  Google Scholar 

  • Ngou BPM, Ding P, Jones JDG (2022) Thirty years of resistance: Zig-zag through the plant immune system. Plant Cell 34:1447–1478

    Article  PubMed  PubMed Central  Google Scholar 

  • Ngou BPM, Wyler M, Schmid MW, Kadota Y, Shirasu K (2024) Evolutionary trajectory of pattern recognition receptors in plants. Nat Commun 15:308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson L, Müller R, Nielsen TH (2007) Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell Environ 30:1499–1512

    Article  CAS  PubMed  Google Scholar 

  • Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi TM, Thibaud M-C (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:83

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N et al (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44:1060–1065

    Article  PubMed  PubMed Central  Google Scholar 

  • Okada K, Yachi K, Nguyen TAN, Kanno S, Tateda C, Lee T-H, Nguyen U, Miyashima S, Hiruma K, Miwa K, et al (2024) Defense-related callose synthase PMR4 promotes root hair callose deposition and adaptation to phosphate deficiency in Arabidopsis thaliana. 2023.07.05.547890. https://doi.org/10.1101/2023.07.05.547890. [PREPRINT]

  • Okazaki Y, Otsuki H, Narisawa T, Kobayashi M, Sawai S, Kamide Y, Kusano M, Aoki T, Hirai MY, Saito K (2013) A new class of plant lipid is essential for protection against phosphorus depletion. Nat Commun 4:1510

    Article  PubMed  Google Scholar 

  • Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263

    Article  CAS  PubMed  Google Scholar 

  • Pandey BK, Verma L, Prusty A, Singh AP, Bennett MJ, Tyagi AK, Giri J, Mehra P (2021) OsJAZ11 regulates phosphate starvation responses in rice. Planta 254:8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pant B-D, Pant P, Erban A, Huhman D, Kopka J, Scheible W-R (2015) Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant Cell Environ 38:172–187

    Article  CAS  PubMed  Google Scholar 

  • Paries M, Gutjahr C (2023) The good, the bad, and the phosphate: regulation of beneficial and detrimental plant–microbe interactions by the plant phosphate status. New Phytol 239:29–46

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 99:13324–13329

  • Paz-Ares J, Puga MI, Rojas-Triana M, Martinez-Hevia I, Diaz S, Poza-Carrión C, Miñambres M, Leyva A (2022) Plant adaptation to low phosphorus availability: Core signaling, crosstalks, and applied implications. Mol Plant 15:104–124

    Article  CAS  PubMed  Google Scholar 

  • Péret B, Desnos T, Jost R, Kanno S, Berkowitz O, Nussaume L (2014) Root architecture responses: in search of phosphate1. Plant Physiol 166:1713–1723

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfeilmeier S, Petti GC, Bortfeld-Miller M, Daniel B, Field CM, Sunagawa S, Vorholt JA (2021) The plant NADPH oxidase RBOHD is required for microbiota homeostasis in leaves. Nat Microbiol 6:852–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeilmeier S, Werz A, Ote M, Bortfeld-Miller M, Kirner P, Keppler A, Hemmerle L, Gäbelein CG, Petti GC, Wolf S et al (2024) Leaf microbiome dysbiosis triggered by T2SS-dependent enzyme secretion from opportunistic Xanthomonas pathogens. Nat Microbiol 9:136–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pruitt RN, Locci F, Wanke F, Zhang L, Saile SC, Joe A, Karelina D, Hua C, Fröhlich K, Wan W-L et al (2021) The EDS1-PAD4-ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature 598:495–499

    Article  CAS  PubMed  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–470

    Article  CAS  PubMed  Google Scholar 

  • Rico-Reséndiz F, Cervantes-Pérez SA, Espinal-Centeno A, Dipp-Álvarez M, Oropeza-Aburto A, Hurtado-Bautista E, Cruz-Hernández A, Bowman JL, Ishizaki K, Arteaga-Vázquez MA et al (2020) Transcriptional and morpho-physiological responses of Marchantia polymorpha upon phosphate starvation. Int J Mol Sci 21:8354

    Article  PubMed  PubMed Central  Google Scholar 

  • Ried MK, Wild R, Zhu J, Pipercevic J, Sturm K, Broger L, Harmel RK, Abriata LA, Hothorn LA, Fiedler D et al (2021) Inositol pyrophosphates promote the interaction of SPX domains with the coiled-coil motif of PHR transcription factors to regulate plant phosphate homeostasis. Nat Commun 12:384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riemer E, Qiu D, Laha D, Harmel RK, Gaugler P, Gaugler V, Frei M, Hajirezaei M-R, Laha NP, Krusenbaum L et al (2021) ITPK1 is an InsP6/ADP phosphotransferase that controls phosphate signaling in Arabidopsis. Mol Plant 14:1864–1880

    Article  CAS  PubMed  Google Scholar 

  • Rouached H, Stefanovic A, Secco D, Bulak Arpat A, Gout E, Bligny R, Poirier Y (2011) Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J 65:557–570

    Article  CAS  PubMed  Google Scholar 

  • Roussin-Léveillée C, Mackey D, Ekanayake G, Gohmann R, Moffett P (2024) Extracellular niche establishment by plant pathogens. Nat Rev Microbiol. https://doi.org/10.1038/s41579-023-00999-8

  • Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Bedoya T, McTavish KJ, Av-Shalom TV, Desveaux D, Guttman DS (2023) Towards integrative plant pathology. Curr Opin Plant Biol 75:102430

    Article  PubMed  Google Scholar 

  • Russ D, Fitzpatrick CR, Teixeira PJPL, Dangl JL (2023) Deep discovery informs difficult deployment in plant microbiome science. Cell 186:4496–4513

    Article  CAS  PubMed  Google Scholar 

  • Rzemieniewski J, Stegmann M (2022) Regulation of pattern-triggered immunity and growth by phytocytokines. Curr Opin Plant Biol 68:102230

    Article  CAS  PubMed  Google Scholar 

  • Saijo Y, Loo EP-I (2020) Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol 225:87–104

    Article  PubMed  Google Scholar 

  • Saijo Y, Loo EP-I, Yasuda S (2018) Pattern recognition receptors and signaling in plant-microbe interactions. Plant J 93:592–613

    Article  CAS  PubMed  Google Scholar 

  • Sasse J, Martinoia E, Northen T (2018) Feed your friends: Do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41

    Article  CAS  PubMed  Google Scholar 

  • Scheible W-R, Pant P, Pant BD, Krom N, Allen RD, Mysore KS (2023) Elucidating the unknown transcriptional responses and PHR1-mediated biotic and abiotic stress tolerance during phosphorus limitation. J Exp Bot 74:2083–2111

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, Wang X, Wang E (2023) Mycorrhizal symbiosis in plant growth and stress adaptation: from genes to ecosystems. Annu Rev Plant Biol 74:569–607

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Zhao B, Zheng S, Zhang X, Wang X, Dong W, Xie Q, Wang G, Xiao Y, Chen F et al (2021) A phosphate starvation response-centered network regulates mycorrhizal symbiosis. Cell 184:5527-5540.e18

    Article  CAS  PubMed  Google Scholar 

  • Smakowska E, Kong J, Busch W, Belkhadir Y (2016) Organ-specific regulation of growth-defense tradeoffs by plants. Curr Opin Plant Biol 29:129–137

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Wilson AJ, Zhang X-C, Thoms D, Sohrabi R, Song S, Geissmann Q, Liu Y, Walgren L, He SY et al (2021) FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat Plants 7:644–654

    Article  CAS  PubMed  Google Scholar 

  • Steffen W, Richardson K, Rockström J, Cornell SE, Fetzer I, Bennett EM, Biggs R, Carpenter SR, de Vries W, de Wit CA et al (2015) Sustainability. Planetary boundaries: guiding human development on a changing planet. Science 347:1259855

    Article  PubMed  Google Scholar 

  • Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel C (2017) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–289

    Article  CAS  PubMed  Google Scholar 

  • Sugio A, MacLean AM, Kingdom HN, Grieve VM, Manimekalai R, Hogenhout SA (2011) Diverse targets of phytoplasma effectors: from plant development to defense against insects. Annu Rev Phytopathol 49:175–195

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Wu D, Li X, Wang L, Xu L, Zhang Y, Xu F, Liu H, Xie Q, Dai S et al (2022) Plant immunity suppression via PHR1-RALF-FERONIA shapes the root microbiome to alleviate phosphate starvation. EMBO J 41:e109102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teixeira PJPL, Colaianni NR, Law TF, Conway JM, Gilbert S, Li H, Salas-González I, Panda D, Del Risco NM, Finkel OM, et al (2021) Specific modulation of the root immune system by a community of commensal bacteria. Proc Natl Acad Sci 118:e2100678118

  • Tian H, Wu Z, Chen S, Ao K, Huang W, Yaghmaiean H, Sun T, Xu F, Zhang Y, Wang S et al (2021) Activation of TIR signalling boosts pattern-triggered immunity. Nature 598:500–503

    Article  CAS  PubMed  Google Scholar 

  • Tintor N, Ross A, Kanehara K, Yamada K, Fan L, Kemmerling B, Nürnberger T, Tsuda K, Saijo Y (2013) Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc Natl Acad Sci U S A 110:6211–6216

  • Toruño TY, Stergiopoulos I, Coaker G (2016) Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu Rev Phytopathol 54:419–441

    Article  PubMed  PubMed Central  Google Scholar 

  • Tzipilevich E, Russ D, Dangl JL, Benfey PN (2021) Plant immune system activation is necessary for efficient root colonization by auxin-secreting beneficial bacteria. Cell Host Microbe 29:1507-1520.e4

    Article  CAS  PubMed  Google Scholar 

  • Val-Torregrosa B, Bundó M, Martín-Cardoso H, Bach-Pages M, Chiou T-J, Flors V, Segundo BS (2022) Phosphate-induced resistance to pathogen infection in Arabidopsis. Plant J 110:452–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Butselaar T, Van den Ackerveken G (2020) Salicylic acid steers the growth-immunity tradeoff. Trends Plant Sci 25:566–576

    Article  PubMed  Google Scholar 

  • Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Snijders R, Kohlen W, Liu J, Bisseling T, Limpens E (2021) Medicago SPX1 and SPX3 regulate phosphate homeostasis, mycorrhizal colonization, and arbuscule degradation. Plant Cell 33:3470–3486

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Shen T, Ni L, Chen C, Jiang J, Cui Z, Wang S, Xu F, Yan R, Jiang M (2023) Phosphorylation of OsRbohB by the protein kinase OsDMI3 promotes H2O2 production to potentiate ABA responses in rice. Mol Plant 16:882–902

    Article  CAS  PubMed  Google Scholar 

  • Wu M, Wei Q, Xu L, Li H, Oelmüller R, Zhang W (2018) Piriformospora indica enhances phosphorus absorption by stimulating acid phosphatase activities and organic acid accumulation in Brassica napus. Plant Soil 432:333–344

    Article  CAS  Google Scholar 

  • Xu L, Zhao H, Wan R, Liu Y, Xu Z, Tian W, Ruan W, Wang F, Deng M, Wang J et al (2019) Identification of vacuolar phosphate efflux transporters in land plants. Nat Plants 5:84–94

    Article  CAS  PubMed  Google Scholar 

  • Yang S-Y, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N et al (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24:4236–4251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S-Y, Lin W-Y, Hsiao Y-M, Chiou T-J (2024) Milestones in understanding transport, sensing, and signaling of the plant nutrient phosphorus. Plant Cell. https://doi.org/10.1093/plcell/koad326

  • Yu H, Xiao A, Dong R, Fan Y, Zhang X, Liu C, Wang C, Zhu H, Duanmu D, Cao Y et al (2018) Suppression of innate immunity mediated by the CDPK-Rboh complex is required for rhizobial colonization in Medicago truncatula nodules. New Phytol 220:425–434

    Article  CAS  PubMed  Google Scholar 

  • Yu K, Liu Y, Tichelaar R, Savant N, Lagendijk E, van Kuijk SJL, Stringlis IA, van Dijken AJH, Pieterse CMJ, Bakker PAHM et al (2019) Rhizosphere-associated Pseudomonas suppress local root immune responses by gluconic acid-mediated lowering of environmental pH. Curr Biol 29:3913-3920.e4

    Article  CAS  PubMed  Google Scholar 

  • Yuan M, Jiang Z, Bi G, Nomura K, Liu M, Wang Y, Cai B, Zhou J-M, He SY, Xin X-F (2021) Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592:105–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Huang L, Hong Y, Song F (2016) Botrytis-induced kinase1, a plasma membrane-localized receptor-like protein kinase, is a negative regulator of phosphate homeostasis in Arabidopsis thaliana. BMC Plant Biol 16:152

  • Zhang L, Hua C, Janocha D, Fliegmann J, Nürnberger T (2023) Plant cell surface immune receptors-Novel insights into function and evolution. Curr Opin Plant Biol 74:102384

    Article  CAS  PubMed  Google Scholar 

  • Zhang X-C, Millet YA, Cheng Z, Bush J, Ausubel FM (2015) Jasmonate signalling in Arabidopsis involves SGT1b-HSP70-HSP90 chaperone complexes. Nat Plants 1:15049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Li T-T, Wang L-F, Guo J-X, Lu K-K, Song R-F, Zuo J-X, Chen H-H, Liu W-C (2022) Abscisic acid facilitates phosphate acquisition through the transcription factor ABA insensitive5 in Arabidopsis. Plant J 111:269–281

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Jia X, Yu N, Murray JD, Yi K, Wang E (2023) Microbe-dependent and independent nitrogen and phosphate acquisition and regulation in plants. New Phytol. https://doi.org/10.1111/nph.19263

  • Zhao H, Sun R, Albrecht U, Padmanabhan C, Wang A, Coffey MD, Girke T, Wang Z, Close TJ, Roose M et al (2013) Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus huanglongbing disease. Mol Plant 6:301–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou F, Emonet A, Dénervaud Tendon V, Marhavy P, Wu D, Lahaye T, Geldner N (2020) Co-incidence of damage and microbial patterns controls localized immune responses in roots. Cell 180:440-453.e18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Hu Q, Xiao X, Yao D, Ge S, Ye J, Li H, Cai R, Liu R, Meng F et al (2021) Mechanism of phosphate sensing and signaling revealed by rice SPX1-PHR2 complex structure. Nat Commun 12:7040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank anonymous reviewers, Kohji Yamada and Kei Hiruma for helpful comments on the manuscript. Our work was supported in part by the grants from the CANON foundation (YS), the Japan Science and Technology Agency (JST, JPMJSC1702 and JPMJTR23UJ (YS)), and MEXT of Japan 22K05650 (KI), 18H02467 and 21H02507 (YS) and 22K05650 (KI).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yusuke Saijo.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Inoue, K., Tsuchida, N. & Saijo, Y. Modulation of plant immunity and biotic interactions under phosphate deficiency. J Plant Res 137, 343–357 (2024). https://doi.org/10.1007/s10265-024-01546-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-024-01546-z

Keywords

Navigation