1932

Abstract

Nutrients are vital to life through intertwined sensing, signaling, and metabolic processes. Emerging research focuses on how distinct nutrient signaling networks integrate and coordinate gene expression, metabolism, growth, and survival. We review the multifaceted roles of sugars, nitrate, and phosphate as essential plant nutrients in controlling complex molecular and cellular mechanisms of dynamic signaling networks. Key advances in central sugar and energy signaling mechanisms mediated by the evolutionarily conserved master regulators HEXOKINASE1 (HXK1), TARGET OF RAPAMYCIN (TOR), and SNF1-RELATED PROTEIN KINASE1 (SNRK1) are discussed. Significant progress in primary nitrate sensing, calcium signaling, transcriptome analysis, and root–shoot communication to shape plant biomass and architecture are elaborated. Discoveries on intracellular and extracellular phosphate signaling and the intimate connections with nitrate and sugar signaling are examined. This review highlights the dynamic nutrient, energy, growth, and stress signaling networks that orchestrate systemwide transcriptional, translational, and metabolic reprogramming, modulate growth and developmental programs, and respond to environmental cues.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-010521-015047
2021-10-06
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/37/1/annurev-cellbio-010521-015047.html?itemId=/content/journals/10.1146/annurev-cellbio-010521-015047&mimeType=html&fmt=ahah

Literature Cited

  1. Aguilera-Alvarado GP, Sánchez-Nieto S. 2017. Plant hexokinases are multifaceted proteins. Plant Cell Physiol 58:1151–60
    [Google Scholar]
  2. Ahn CS, Han J-A, Lee H-S, Lee S, Pai H-S. 2011. The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell 23:185–209
    [Google Scholar]
  3. Alvarez JM, Moyano TC, Zhang T, Gras DE, Herrera FJ et al. 2019. Local changes in chromatin accessibility and transcriptional networks underlying the nitrate response in Arabidopsis roots. Mol. Plant 12:1545–60
    [Google Scholar]
  4. Alvarez JM, Schinke A-L, Brooks MD, Pasquino A, Leonelli L et al. 2020. Transient genome-wide interactions of the master transcription factor NLP7 initiate a rapid nitrogen-response cascade. Nat. Commun. 11:1157
    [Google Scholar]
  5. Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S et al. 2014. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. PNAS 111:2029–34
    [Google Scholar]
  6. Baena-González E, Lunn JE. 2020. SnRK1 and trehalose 6-phosphate—two ancient pathways converge to regulate plant metabolism and growth. Curr. Opin. Plant Biol. 55:52–59
    [Google Scholar]
  7. Baena-González E, Rolland F, Thevelein JM, Sheen J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–42
    [Google Scholar]
  8. Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C et al. 2017. Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat. Commun. 8:15300
    [Google Scholar]
  9. Bari R, Pant BD, Stitt M, Scheible W-R. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–99
    [Google Scholar]
  10. Barrada A, Djendli M, Desnos T, Mercier R, Robaglia C et al. 2019. A TOR-YAK1 signaling axis controls cell cycle, meristem activity and plant growth in Arabidopsis. Development 146:dev171298
    [Google Scholar]
  11. Bhosale R, Giri J, Pandey BK, Giehl RF, Hartmann A et al. 2018. A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat. Commun. 9:1409
    [Google Scholar]
  12. Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M et al. 2015. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 1:15015
    [Google Scholar]
  13. Broeckx T, Hulsmans S, Rolland F 2016. The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function. J. Exp. Bot. 67:6215–52
    [Google Scholar]
  14. Brooks MD, Cirrone J, Pasquino AV, Alvarez JM, Swift J et al. 2019. Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions. Nat. Commun. 10:1569
    [Google Scholar]
  15. Bruggeman Q, Prunier F, Mazubert C, de Bont L, Garmier M et al. 2015. Involvement of Arabidopsis hexokinase1 in cell death mediated by myo-inositol accumulation. Plant Cell 27:1801–14
    [Google Scholar]
  16. Brunkard JO, Xu M, Scarpin MR, Chatterjee S, Shemyakina EA et al. 2020. TOR dynamically regulates plant cell–cell transport. PNAS 117:5049–58
    [Google Scholar]
  17. Bruns AN, Li S, Mohannath G, Bisaro DM. 2019. Phosphorylation of Arabidopsis eIF4E and eIFiso4E by SnRK1 inhibits translation. FEBS J 286:3778–96
    [Google Scholar]
  18. Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V et al. 2010. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLOS Genet 6:e1001102
    [Google Scholar]
  19. Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L et al. 2013. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J 73:897–909
    [Google Scholar]
  20. Canales J, Moyano TC, Villarroel E, Gutiérrez RA. 2014. Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front. Plant Sci. 5:22
    [Google Scholar]
  21. Cao P, Kim S-J, Xing A, Schenck CA, Liu L et al. 2019. Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis. eLife 8:e50747
    [Google Scholar]
  22. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y et al. 2009. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–35
    [Google Scholar]
  23. Chen G-H, Liu M-J, Xiong Y, Sheen J, Wu S-H 2018. TOR and RPS6 transmit light signals to enhance protein translation in deetiolating Arabidopsis seedlings. PNAS 115:12823–28
    [Google Scholar]
  24. Chen H-Y, Lin S-H, Cheng L-H, Wu J-J, Lin Y-C et al. 2021. Potential transceptor AtNRT1.13 modulates shoot architecture and flowering time in a nitrate-dependent manner. Plant Cell https://doi.org/10.1093/plcell/koab051
    [Crossref] [Google Scholar]
  25. Chen L, Su Z-Z, Huang L, Xia F-N, Qi H et al. 2017. The AMP-activated protein kinase KIN10 is involved in the regulation of autophagy in Arabidopsis. Front. Plant Sci. 8:1201
    [Google Scholar]
  26. Chen L-Q, Cheung LS, Feng L, Tanner W, Frommer WB. 2015. Transport of sugars. Annu. Rev. Biochem. 84:865–94
    [Google Scholar]
  27. Chien P-S, Chiang C-P, Leong SJ, Chiou T-J. 2018. Sensing and signaling of phosphate starvation: from local to long distance. Plant Cell Physiol 59:1714–22
    [Google Scholar]
  28. Chiou T-J, Aung K, Lin S-I, Wu C-C, Chiang S-F, Su C-I. 2006. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–21
    [Google Scholar]
  29. Cho H-Y, Lu M-YJ, Shih M-C. 2019. The SnRK1-eIFiso4G1 signaling relay regulates the translation of specific mRNAs in Arabidopsis under submergence. New Phytol 222:366–81
    [Google Scholar]
  30. Cho H-Y, Wen T-N, Wang Y-T, Shih M-C. 2016. Quantitative phosphoproteomics of protein kinase SnRK1 regulated protein phosphorylation in Arabidopsis under submergence. J. Exp. Bot. 67:2745–60
    [Google Scholar]
  31. Cho J-I, Ryoo N, Eom J-S, Lee D-W, Kim H-B et al. 2009. Role of the rice hexokinases OsHXK5 and OsHXK6 as glucose sensors. Plant Physiol 149:745–59
    [Google Scholar]
  32. Cho Y-H, Yoo S-D. 2011. Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLOS Genet 7:e1001263
    [Google Scholar]
  33. Cho Y-H, Yoo S-D, Sheen J. 2006. Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–89
    [Google Scholar]
  34. Claeys H, Vi SL, Xu X, Satoh-Nagasawa N, Eveland AL et al. 2019. Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity. Nat. Plants 5:352
    [Google Scholar]
  35. Couso I, Pérez-Pérez ME, Ford MM, Martínez-Force E, Hicks LM et al. 2020. Phosphorus availability regulates TORC1 signaling via LST8 in Chlamydomonas. Plant Cell 32:69–80
    [Google Scholar]
  36. Deprost D, Yao L, Sormani R, Moreau M, Leterreux G et al. 2007. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–70
    [Google Scholar]
  37. Dobrenel T, Caldana C, Hanson J, Robaglia C, Vincentz M et al. 2016. TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67:261–85
    [Google Scholar]
  38. Dong J, Ma G, Sui L, Wei M, Satheesh V et al. 2019. Inositol pyrophosphate InsP8 acts as an intracellular phosphate signal in Arabidopsis. Mol. Plant 12:1463–73
    [Google Scholar]
  39. Dong J, Piñeros MA, Li X, Yang H, Liu Y et al. 2017. An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots. Mol. Plant 10:244–59
    [Google Scholar]
  40. Dong Y, Silbermann M, Speiser A, Forieri I, Linster E et al. 2017. Sulfur availability regulates plant growth via glucose-TOR signaling. Nat. Commun. 8:1174
    [Google Scholar]
  41. Eastmond PJ, Van Dijken AJ, Spielman M, Kerr A, Tissier AF et al. 2002. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29:225–35
    [Google Scholar]
  42. Emanuelle S, Hossain MI, Moller IE, Pedersen HL, Meene AM et al. 2015. SnRK1 from Arabidopsis thaliana is an atypical AMPK. Plant J 82:183–92
    [Google Scholar]
  43. Enganti R, Cho SK, Toperzer JD, Urquidi-Camacho RA, Cakir OS et al. 2018. Phosphorylation of ribosomal protein RPS6 integrates light signals and circadian clock signals. Front. Plant Sci. 8:2210
    [Google Scholar]
  44. Feng J, Zhao S, Chen X, Wang W, Dong W et al. 2015. Biochemical and structural study of Arabidopsis hexokinase 1. Acta Crystallogr. Sect. D 71:367–75
    [Google Scholar]
  45. Fichtner F, Olas JJ, Feil R, Watanabe M, Krause U et al. 2020. Functional features of TREHALOSE-6-PHOSPHATE SYNTHASE1, an essential enzyme in Arabidopsis. Plant Cell 32:1949–72
    [Google Scholar]
  46. Figueroa CM, Lunn JE. 2016. A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol 172:7–27
    [Google Scholar]
  47. Forzani C, Duarte GT, Van Leene J, Clément G, Huguet S et al. 2019. Mutations of the AtYAK1 kinase suppress TOR deficiency in Arabidopsis. Cell Rep 27:3696–708.e5
    [Google Scholar]
  48. Frank A, Matiolli CC, Viana AJ, Hearn TJ, Kusakina J et al. 2018. Circadian entrainment in Arabidopsis by the sugar-responsive transcription factor bZIP63. Curr. Biol. 28:2597–606.e6
    [Google Scholar]
  49. Fu L, Liu Y, Qin G, Wu P, Zi H et al. 2021. The TOR–EIN2 axis mediates nuclear signalling to modulate plant growth. Nature 591:28892
    [Google Scholar]
  50. Gaudinier A, Rodriguez-Medina J, Zhang L, Olson A, Liseron-Monfils C et al. 2018. Transcriptional regulation of nitrogen-associated metabolism and growth. Nature 563:259–64
    [Google Scholar]
  51. Godon C, Mercier C, Wang X, David P, Richaud P et al. 2019. Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells. Plant J 99:937–49
    [Google Scholar]
  52. Griffiths CA, Sagar R, Geng Y, Primavesi LF, Patel MK et al. 2016. Chemical intervention in plant sugar signalling increases yield and resilience. Nature 540:574–78
    [Google Scholar]
  53. Guan P, Ripoll J-J, Wang R, Vuong L, Bailey-Steinitz LJ et al. 2017. Interacting TCP and NLP transcription factors control plant responses to nitrate availability. PNAS 114:2419–24
    [Google Scholar]
  54. Gutiérrez-Alanís D, Yong-Villalobos L, Jiménez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A et al. 2017. Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev. Cell 41:555–70.e3
    [Google Scholar]
  55. Ham B-K, Chen J, Yan Y, Lucas WJ 2018. Insights into plant phosphate sensing and signaling. Curr. Opin. Biotechnol. 49:1–9
    [Google Scholar]
  56. Han C, Liu Y, Shi W, Qiao Y, Wang L et al. 2020. KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor. Nat. Commun. 11:4214
    [Google Scholar]
  57. Ho C-H, Lin S-H, Hu H-C, Tsay Y-F. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138:1184–94
    [Google Scholar]
  58. Hu B, Jiang Z, Wang W, Qiu Y, Zhang Z et al. 2019. Nitrate–NRT1.1B–SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat. Plants 5:401
    [Google Scholar]
  59. Hu D-G, Sun C-H, Zhang Q-Y, An J-P, You C-X, Hao Y-J 2016. Glucose sensor MdHXK1 phosphorylates and stabilizes MdbHLH3 to promote anthocyanin biosynthesis in apple. PLOS Genet 12:e1006273
    [Google Scholar]
  60. Huang J-P, Tunc-Ozdemir M, Chang Y, Jones AM 2015. Cooperative control between AtRGS1 and AtHXK1 in a WD40-repeat protein pathway in Arabidopsis thaliana. Front. Plant Sci. 6:851
    [Google Scholar]
  61. Huang T-K, Han C-L, Lin S-I, Chen Y-J, Tsai Y-C et al. 2013. Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25:4044–60
    [Google Scholar]
  62. Hwang G, Kim S, Cho J-Y, Paik I, Kim J-I, Oh E. 2019. Trehalose-6-phosphate signaling regulates thermoresponsive hypocotyl growth in Arabidopsis thaliana. EMBO Rep 20:e47828
    [Google Scholar]
  63. Im JH, Cho YH, Kim GD, Kang GH, Hong JW, Yoo SD. 2014. Inverse modulation of the energy sensor Snf1-related protein kinase 1 on hypoxia adaptation and salt stress tolerance in Arabidopsis thaliana. Plant Cell Environ 37:2303–12
    [Google Scholar]
  64. Jamsheer KM, Sharma M, Singh D, Mannully CT, Jindal S et al. 2018. FCS-like zinc finger 6 and 10 repress SnRK 1 signalling in Arabidopsis. Plant J 94:232–45
    [Google Scholar]
  65. Jang J-C, León P, Zhou L, Sheen J. 1997. Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19
    [Google Scholar]
  66. Jeong E-Y, Seo PJ, Woo JC, Park C-M. 2015. AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis. BMC Plant Biol 15:110
    [Google Scholar]
  67. Jossier M, Bouly JP, Meimoun P, Arjmand A, Lessard P et al. 2009. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59:316–28
    [Google Scholar]
  68. Kant S, Peng M, Rothstein SJ. 2011. Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLOS Genet 7:e1002021
    [Google Scholar]
  69. Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB et al. 2008. Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228:411
    [Google Scholar]
  70. Kelly G, David-Schwartz R, Sade N, Moshelion M, Levi A et al. 2012. The pitfalls of transgenic selection and new roles of AtHXK1: A high level of AtHXK1 expression uncouples hexokinase1-dependent sugar signaling from exogenous sugar. Plant Physiol 159:47–51
    [Google Scholar]
  71. Kiba T, Inaba J, Kudo T, Ueda N, Konishi M et al. 2018. Repression of nitrogen starvation responses by members of the Arabidopsis GARP-type transcription factor NIGT1/HRS1 subfamily. Plant Cell 30:925–45
    [Google Scholar]
  72. Kim G-D, Cho Y-H, Yoo S-D. 2017. Regulatory functions of cellular energy sensor SNF1-Related Kinase1 for leaf senescence delay through ETHYLENE-INSENSITIVE3 repression. Sci. Rep. 7:3193
    [Google Scholar]
  73. Konishi M, Yanagisawa S. 2013. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat. Commun. 4:1617
    [Google Scholar]
  74. Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A et al. 2011. Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol 157:1255–82
    [Google Scholar]
  75. Lee D-H, Park SJ, Ahn CS, Pai H-S. 2017. MRF family genes are involved in translation control, especially under energy-deficient conditions, and their expression and functions are modulated by the TOR signaling pathway. Plant Cell 29:2895–920
    [Google Scholar]
  76. Lei M, Liu Y, Zhang B, Zhao Y, Wang X et al. 2011. Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol 156:1116–30
    [Google Scholar]
  77. Léran S, Edel KH, Pervent M, Hashimoto K, Corratgé-Faillie C et al. 2015. Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci. Signal. 8:ra43
    [Google Scholar]
  78. Li L, Sheen J. 2016. Dynamic and diverse sugar signaling. Curr. Opin. Plant Biol. 33:116–25
    [Google Scholar]
  79. Li P, Wind JJ, Shi X, Zhang H, Hanson J et al. 2011. Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. PNAS 108:3436–41
    [Google Scholar]
  80. Li S, Tian Y, Wu K, Ye Y, Yu J et al. 2018. Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560:595–600
    [Google Scholar]
  81. Li X, Cai W, Liu Y, Li H, Fu L et al. 2017. Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. PNAS 114:2765–70
    [Google Scholar]
  82. Lin S-I, Chiang S-F, Lin W-Y, Chen J-W, Tseng C-Y et al. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–46
    [Google Scholar]
  83. 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 25:4061–74
    [Google Scholar]
  84. Liu K-H, Diener A, Lin Z, Liu C, Sheen J. 2020. Primary nitrate responses mediated by calcium signalling and diverse protein phosphorylation. J. Exp. Bot. 71:4428–41
    [Google Scholar]
  85. Liu K-H, Niu Y, Konishi M, Wu Y, Du H et al. 2017. Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 545:311–16
    [Google Scholar]
  86. Liu T-Y, Huang T-K, Tseng C-Y, Lai Y-S, Lin S-I et al. 2012. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24:2168–83
    [Google Scholar]
  87. Liu Y, Duan X, Zhao X, Ding W, Wang Y et al. 2021. Diverse nitrogen signals activate convergent ROP2-TOR signaling in Arabidopsis. . Dev. Cell 56:128395.e5
    [Google Scholar]
  88. Maeda Y, Konishi M, Kiba T, Sakuraba Y, Sawaki N et al. 2018. A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat. Commun. 9:1376
    [Google Scholar]
  89. Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A et al. 2015. SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife 4:e05828
    [Google Scholar]
  90. Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E et al. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4:1713
    [Google Scholar]
  91. Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R et al. 2015. AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat. Commun. 6:6274
    [Google Scholar]
  92. Medici A, Szponarski W, Dangeville P, Safi A, Dissanayake IM et al. 2019. Identification of molecular integrators shows that nitrogen actively controls the phosphate starvation response in plants. Plant Cell 31:1171–84
    [Google Scholar]
  93. Menand B, Desnos T, Nussaume L, Berger F, Bouchez D et al. 2002. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. PNAS 99:6422–27
    [Google Scholar]
  94. Mohammed B, Bilooei SF, Dóczi R, Grove E, Railo S et al. 2018. Converging light, energy and hormonal signaling control meristem activity, leaf initiation, and growth. Plant Physiol 176:1365–81
    [Google Scholar]
  95. Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H et al. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–36
    [Google Scholar]
  96. Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A et al. 2017. Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. PNAS 114:E3563–72
    [Google Scholar]
  97. Moreau M, Azzopardi M, Clément G, Dobrenel T, Marchive C et al. 2012. Mutations in the Arabidopsis homolog of LST8/GβL, a partner of the target of rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24:463–81
    [Google Scholar]
  98. Müller J, Toev T, Heisters M, Teller J, Moore KL et al. 2015. Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev. Cell 33:216–30
    [Google Scholar]
  99. Müller R, Morant M, Jarmer H, Nilsson L, Nielsen TH. 2007. Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–71
    [Google Scholar]
  100. Naulin PA, Armijo GI, Vega AS, Tamayo KP, Gras DE et al. 2020. Nitrate induction of primary root growth requires cytokinin signaling in Arabidopsis thaliana. Plant Cell Physiol 61:342–52
    [Google Scholar]
  101. Nukarinen E, Nägele T, Pedrotti L, Wurzinger B, Mair A et al. 2016. Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation. Sci. Rep. 6:31697
    [Google Scholar]
  102. Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ et al. 2013. Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol. Biochem. 63:89–98
    [Google Scholar]
  103. O'Leary BM, Oh GGK, Lee CP, Millar AH. 2020. Metabolite regulatory interactions control plant respiratory metabolism via Target of Rapamycin (TOR) kinase activation. Plant Cell 32:666–82
    [Google Scholar]
  104. Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y. 2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat. Plants 3:17029
    [Google Scholar]
  105. Pedrotti L, Weiste C, Nägele T, Wolf E, Lorenzin F et al. 2018. Snf1-RELATED KINASE1-controlled C/S1-bZIP signaling activates alternative mitochondrial metabolic pathways to ensure plant survival in extended darkness. Plant Cell 30:495–509
    [Google Scholar]
  106. Pérez-Torres C-A, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S et al. 2008. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–72
    [Google Scholar]
  107. Pfeiffer A, Janocha D, Dong Y, Medzihradszky A, Schöne S et al. 2016. Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. eLife 5:e17023
    [Google Scholar]
  108. Puga MI, Mateos I, Charukesi R, Wang Z, Franco-Zorrilla JM et al. 2014. SPX1 is a phosphate-dependent inhibitor of Phosphate Starvation Response 1 in Arabidopsis. PNAS 111:14947–52
    [Google Scholar]
  109. Puga MI, Rojas-Triana M, de Lorenzo L, Leyva A, Rubio V, Paz-Ares J. 2017. Novel signals in the regulation of Pi starvation responses in plants: facts and promises. Curr. Opin. Plant Biol. 39:40–49
    [Google Scholar]
  110. Raghothama K. 2000. Phosphate transport and signaling. Curr. Opin. Plant Biol. 3:182–87
    [Google Scholar]
  111. Rahmani F, Hummel M, Schuurmans J, Wiese-Klinkenberg A, Smeekens S, Hanson J. 2009. Sucrose control of translation mediated by an upstream open reading frame-encoded peptide. Plant Physiol 150:1356–67
    [Google Scholar]
  112. Ramon M, Dang TVT, Broeckx T, Hulsmans S, Crepin N et al. 2019. Default activation and nuclear translocation of the plant cellular energy sensor SnRK1 regulate metabolic stress responses and development. Plant Cell 31:1614–32
    [Google Scholar]
  113. Ramon M, Ruelens P, Li Y, Sheen J, Geuten K, Rolland F 2013. The hybrid Four-CBS-Domain KINβγ subunit functions as the canonical γ subunit of the plant energy sensor SnRK1. Plant J 75:11–25
    [Google Scholar]
  114. Ren M, Qiu S, Venglat P, Xiang D, Feng L et al. 2011. Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol 155:1367–82
    [Google Scholar]
  115. Ren M, Venglat P, Qiu S, Feng L, Cao Y et al. 2012. Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24:4850–74
    [Google Scholar]
  116. Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA. 2015. The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol 169:1397–404
    [Google Scholar]
  117. Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A et al. 2013. ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25:3871–84
    [Google Scholar]
  118. Rolland F, Baena-Gonzalez E, Sheen J. 2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57:675–709
    [Google Scholar]
  119. Roth MS, Westcott DJ, Iwai M, Niyogi KK. 2019. Hexokinase is necessary for glucose-mediated photosynthesis repression and lipid accumulation in a green alga. Commun. Biol. 2:347
    [Google Scholar]
  120. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J et al. 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–33
    [Google Scholar]
  121. Ruiz-Gayosso A, Rodríguez-Sotres R, Martínez-Barajas E, Coello P. 2018. A role for the carbohydrate-binding module (CBM) in regulatory SnRK1 subunits: the effect of maltose on SnRK1 activity. Plant J 96:163–75
    [Google Scholar]
  122. Ryabova LA, Robaglia C, Meyer C. 2019. Target of Rapamycin kinase: central regulatory hub for plant growth and metabolism. J. Exp. Bot. 70:2211
    [Google Scholar]
  123. Sakakibara H. 2020. Cytokinin biosynthesis and transport for systemic nitrogen signaling. Plant J.
    [Google Scholar]
  124. Sakakibara H, Kobayashi K, Deji A, Sugiyama T. 1997. Partial characterization of the signaling pathway for the nitrate-dependent expression of genes for nitrogen-assimilatory enzymes using detached maize leaves. Plant Cell Physiol 38:837–43
    [Google Scholar]
  125. Scarpin MR, Leiboff S, Brunkard JO 2020. Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation. eLife 9:e58795
    [Google Scholar]
  126. Scheible W-R, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M. 1997. Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–98
    [Google Scholar]
  127. Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D et al. 2004. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–99
    [Google Scholar]
  128. Schepetilnikov M, Dimitrova M, Mancera-Martínez E, Geldreich A, Keller M, Ryabova LA. 2013. TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J 32:1087–102
    [Google Scholar]
  129. Schepetilnikov M, Makarian J, Srour O, Geldreich A, Yang Z et al. 2017. GTPase ROP2 binds and promotes activation of target of rapamycin, TOR, in response to auxin. EMBO J 36:886–903
    [Google Scholar]
  130. Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M 2003. Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. PNAS 100:6849–54
    [Google Scholar]
  131. Sheen J. 2014. Master regulators in plant glucose signaling networks. J. Plant Biol. 57:67–79
    [Google Scholar]
  132. Shen W, Reyes MI, Hanley-Bowdoin L. 2009. Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop. Plant Physiol 150:996–1005
    [Google Scholar]
  133. Shi L, Wu Y, Sheen J. 2018. TOR signaling in plants: conservation and innovation. Development 145:dev160887
    [Google Scholar]
  134. Soto-Burgos J, Zhuang X, Jiang L, Bassham DC. 2018. Dynamics of autophagosome formation. Plant Physiol 176:219–29
    [Google Scholar]
  135. Stein O, Granot D. 2019. An overview of sucrose synthases in plants. Front. Plant Sci. 10:95
    [Google Scholar]
  136. Sun L, Song L, Zhang Y, Zheng Z, Liu D. 2016. Arabidopsis PHL2 and PHR1 act redundantly as the key components of the central regulatory system controlling transcriptional responses to phosphate starvation. Plant Physiol 170:499–514
    [Google Scholar]
  137. Swift J, Alvarez JM, Araus V, Gutiérrez RA, Coruzzi GM 2020. Nutrient dose-responsive transcriptome changes driven by Michaelis–Menten kinetics underlie plant growth rates. PNAS 117:12531–40
    [Google Scholar]
  138. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46
    [Google Scholar]
  139. Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A et al. 2010. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–89
    [Google Scholar]
  140. Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 1:15025
    [Google Scholar]
  141. Tsai AYL, Gazzarrini S. 2012. AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis. Plant J 69:809–21
    [Google Scholar]
  142. Ueda Y, Kiba T, Yanagisawa S. 2020. Nitrate-inducible NIGT1 proteins modulate phosphate uptake and starvation signalling via transcriptional regulation of SPX genes. Plant J 102:448–66
    [Google Scholar]
  143. Ulfstedt M, Hu G-Z, Eklund DM, Ronne H. 2018. The ability of a charophyte alga hexokinase to restore glucose signaling and glucose repression of gene expression in a glucose-insensitive Arabidopsis hexokinase mutant depends on its catalytic activity. Front. Plant Sci. 9:1887
    [Google Scholar]
  144. Urano D, Phan N, Jones JC, Yang J, Huang J et al. 2012. Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nat. Cell Biol. 14:1079–88
    [Google Scholar]
  145. Van Leene J, Han C, Gadeyne A, Eeckhout D, Matthijs C et al. 2019. Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nat. Plants 5:316–27
    [Google Scholar]
  146. Varala K, Marshall-Colón A, Cirrone J, Brooks MD, Pasquino AV et al. 2018. Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants. PNAS 115:6494–99
    [Google Scholar]
  147. Vidal EA, Alvarez JM, Araus V, Riveras E, Brooks M et al. 2020. Nitrate in 2020: thirty years from transport to signaling networks. Plant Cell 32:2094–119
    [Google Scholar]
  148. Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA 2013. Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. PNAS 110:12840–45
    [Google Scholar]
  149. Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T et al. 2013. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–7
    [Google Scholar]
  150. Walker L, Boddington C, Jenkins D, Wang Y, Grønlund JT et al. 2017. Changes in gene expression in space and time orchestrate environmentally mediated shaping of root architecture. Plant Cell 29:2393–412
    [Google Scholar]
  151. Wang P, Zhao Y, Li Z, Hsu C-C, Liu X et al. 2018. Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol. Cell 69:100–12.e6
    [Google Scholar]
  152. Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X et al. 2004. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136:2512–22
    [Google Scholar]
  153. Wang X, Feng C, Tian L, Hou C, Tian W et al. 2021. A transceptor-channel complex couples nitrate sensing to calcium signaling in Arabidopsis. Mol. Plant 14:P77486
    [Google Scholar]
  154. Wang Y-Y, Cheng Y-H, Chen K-E, Tsay Y-F. 2018. Nitrate transport, signaling, and use efficiency. Annu. Rev. Plant Biol. 69:85–122
    [Google Scholar]
  155. Wang Z, Ruan W, Shi J, Zhang L, Xiang D et al. 2014. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. PNAS 111:14953–58
    [Google Scholar]
  156. Wege S, Khan GA, Jung J-Y, Vogiatzaki E, Pradervand S et al. 2016. The EXS domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal. Plant Physiol 170:385–400
    [Google Scholar]
  157. Wendrich JR, Yang B, Vandamme N, Verstaen K, Smet W et al. 2020. Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions. Science 370:eaay4970
    [Google Scholar]
  158. Wild R, Gerasimaite R, Jung J-Y, Truffault V, Pavlovic I et al. 2016. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science 352:986–90
    [Google Scholar]
  159. Wu K, Wang S, Song W, Zhang J, Wang Y et al. 2020. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367:eaaz2046
    [Google Scholar]
  160. Wu Y, Shi L, Li L, Fu L, Liu Y et al. 2019. Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J. Exp. Bot. 70:2227–38
    [Google Scholar]
  161. Xiong F, Zhang R, Meng Z, Deng K, Que Y et al. 2017. Brassinosteriod Insensitive 2 (BIN2) acts as a downstream effector of the Target of Rapamycin (TOR) signaling pathway to regulate photoautotrophic growth in Arabidopsis. New Phytol 213:233–49
    [Google Scholar]
  162. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J. 2013. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–86
    [Google Scholar]
  163. Xiong Y, Sheen J. 2012. Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J. Biol. Chem. 287:2836–42
    [Google Scholar]
  164. Xu S-L, Chalkley RJ, Maynard JC, Wang W, Ni W et al. 2017. Proteomic analysis reveals O-GlcNAc modification on proteins with key regulatory functions in Arabidopsis. PNAS 114:E1536–43
    [Google Scholar]
  165. Yan D, Easwaran V, Chau V, Okamoto M, Ierullo M et al. 2016. NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nat. Commun. 7:13179
    [Google Scholar]
  166. Yanagisawa S, Yoo S-D, Sheen J. 2003. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–25
    [Google Scholar]
  167. Zentella R, Hu J, Hsieh W-P, Matsumoto PA, Dawdy A et al. 2016. O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis. Genes Dev 30:164–76
    [Google Scholar]
  168. Zentella R, Sui N, Barnhill B, Hsieh W-P, Hu J et al. 2017. The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA. Nat. Chem. Biol. 13:479–85
    [Google Scholar]
  169. Zhai Z, Keereetaweep J, Liu H, Feil R, Lunn JE, Shanklin J. 2018. Trehalose 6-phosphate positively regulates fatty acid synthesis by stabilizing WRINKLED1. Plant Cell 30:2616–27
    [Google Scholar]
  170. Zhai Z, Liu H, Shanklin J. 2017. Phosphorylation of WRINKLED1 by KIN10 results in its proteasomal degradation, providing a link between energy homeostasis and lipid biosynthesis. Plant Cell 29:871–89
    [Google Scholar]
  171. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–9
    [Google Scholar]
  172. Zhang N, Meng Y, Li X, Zhou Y, Ma L et al. 2019. Metabolite-mediated TOR signaling regulates the circadian clock in Arabidopsis. PNAS 116:25395–97
    [Google Scholar]
  173. Zhang X, Cui Y, Yu M, Su B, Gong W et al. 2019. Phosphorylation-mediated dynamics of nitrate transceptor NRT1.1 regulate auxin flux and nitrate signaling in lateral root growth. Plant Physiol 181:480–98
    [Google Scholar]
  174. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA et al. 2009. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–71
    [Google Scholar]
  175. Zhang Z, Zheng Y, Ham B-K, Chen J, Yoshida A et al. 2016a. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat. Plants 2:16033
    [Google Scholar]
  176. Zhang Z, Zhu J-Y, Roh J, Marchive C, Kim S-K et al. 2016b. TOR signaling promotes accumulation of BZR1 to balance growth with carbon availability in Arabidopsis. Curr. Biol. 26:1854–60
    [Google Scholar]
  177. Zhu J, Lau K, Puschmann R, Harmel RK, Zhang Y et al. 2019. Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis. eLife 8:e43582
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-010521-015047
Loading
/content/journals/10.1146/annurev-cellbio-010521-015047
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error