1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 74, 2023
  5. Article

Annual Review of Plant Biology

Volume 74, 2023

Plant Hormone Transport and Localization: Signaling Molecules on the Move

Abstract

Plant hormones are a group of small signaling molecules produced by plants at very low concentrations that have the ability to move and function at distal sites. Hormone homeostasis is critical to balance plant growth and development and is regulated at multiple levels, including hormone biosynthesis, catabolism, perception, and transduction. In addition, plants move hormones over short and long distances to regulate various developmental processes and responses to environmental factors. Transporters coordinate these movements, resulting in hormone maxima, gradients, and cellular and subcellular sinks. Here, we summarize the current knowledge of most of the characterized plant hormone transporters with respect to biochemical, physiological, and developmental activities. We further discuss the subcellular localizations of transporters, their substrate specificities, and the need for multiple transporters for the same hormone in the context of plant growth and development.

Keyword(s): ABA, abscisic acid, auxin, CK, cytokinin, ethylene, GA, gibberellin, hormone homeostasis, IAA, JA, jasmonic acid, phytohormones, plant hormones, transport mechanisms, transporter
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070722-015329
2023-05-22
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/arplant/74/1/annurev-arplant-070722-015329.html?itemId=/content/journals/10.1146/annurev-arplant-070722-015329&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abualia R, Benkova E, Lacombe B. 2018. Transporters and mechanisms of hormone transport in Arabidopsis. Adv. Bot. Rev. 87:115–38
     [Google Scholar]
  2. 2.
    Adamowski M, Friml J. 2015. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32
     [Google Scholar]
  3. 3.
    Aida M, Vernoux T, Furutani M, Traas J, Tasaka M. 2002. Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129:3965–74
     [Google Scholar]
  4. 4.
    Anfang M, Shani E 2021. Transport mechanisms of plant hormones. Curr. Opin. Plant Biol. 63:102055Review summarizing plant hormone transporters and hormone transport mechanisms.
     [Google Scholar]
  5. 5.
    Aryal B, Huynh J, Schneuwly J, Siffert A, Liu J et al. 2019. ABCG36/PEN3/PDR8 is an exporter of the auxin precursor, indole-3-butyric acid, and involved in auxin-controlled development. Front. Plant Sci. 10:899
     [Google Scholar]
  6. 6.
    Balcerowicz M, Shetty KN, Jones AM. 2021. Fluorescent biosensors illuminating plant hormone research. Plant Physiol. 187:590–602
     [Google Scholar]
  7. 7.
    Barbosa ICR, Hammes UZ, Schwechheimer C. 2018. Activation and polarity control of PIN-FORMED auxin transporters by phosphorylation. Trends Plant Sci. 23:6523–38
     [Google Scholar]
  8. 8.
    Barker R, Garcia MNF, Powers SJ, Vaughan S, Bennett MJ et al. 2021. Mapping sites of gibberellin biosynthesis in the Arabidopsis root tip. New Phytol. 229:1521–34
     [Google Scholar]
  9. 9.
    Bennett MJ, Marchant A, Green HG, May ST, Ward SP et al. 1996. Arabidopsis AUX1 gene: a permease-like regulator root gravitropism. Science 273:948–50
     [Google Scholar]
  10. 10.
    Binenbaum J, Weinstain R, Shani E 2018. Gibberellin localization and transport in plants. Trends Plant Sci. 23:5410–21
     [Google Scholar]
  11. 11.
    Binenbaum J, Wulff N, Camut L, Kiradjiev K, Anfang M et al. 2023. Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis. Nat. Plants In press https://doi.org/10.1038/s41477-023-01391-3
    [Crossref] [Google Scholar]
  12. 12.
    Borlaug N. 1968. Wheat breeding and its impact on world food supply. Proceedings of the 3rd International Wheat Genetics Symposium, Canberra, Aust., August 5–91–36. Canberra, Aust.: Aust. Acad. Sci. Canberra
     [Google Scholar]
  13. 13.
    Boyer GL, Zeevaart JAD. 1982. Isolation and quantitation of β-d-glucopyranosyl abscisate from leaves of Xanthium and spinach. Plant Physiol. 70:227–31
     [Google Scholar]
  14. 14.
    Breitel DA, Chappell-Maor L, Meir S, Panizel I, Puig CP et al. 2016. AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLOS Genet. 12:3e1005903
     [Google Scholar]
  15. 15.
    Brumos J, Robles LM, Yun J, Vu TC, Jackson S et al. 2018. Local auxin biosynthesis is a key regulator of plant development. Dev. Cell 47:306–18
     [Google Scholar]
  16. 16.
    Bürkle L, Cedzich A, Döpke C, Stransky H, Okumoto S et al. 2003. Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis. Plant J. 34:13–26
     [Google Scholar]
  17. 17.
    Burla B, Pfrunder S, Nagy R, Francisco RM, Lee Y, Martinoia E. 2013. Vacuolar transport of abscisic acid glucosyl ester is mediated by ATP-binding cassette and proton-antiport mechanisms in Arabidopsis. Plant Physiol. 163:1446–58
     [Google Scholar]
  18. 18.
    Cazzonelli CI, Vanstraelen M, Simon S, Yin K, Carron-Arthur A et al. 2013. Role of the Arabidopsis PIN6 auxin transporter in auxin homeostasis and auxin-mediated development. PLOS ONE 8:7e70069
     [Google Scholar]
  19. 19.
    Chen J, Hu Y, Hao P, Tsering T, Xia J et al. 2023. ABCB-mediated shootward auxin transport feeds into the root clock. EMBO Rep. 2023:e56271Shows that five ABCB auxin transporters act redundantly to transport IAA to regulate lateral root spacing.
     [Google Scholar]
  20. 20.
    Chen Q, Dai X, De-Paoli H, Cheng Y, Takebayashi Y et al. 2014. Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 55:61072–79
     [Google Scholar]
  21. 21.
    Chiba Y, Shimizu T, Miyakawa S, Kanno Y, Koshiba T et al. 2015. Identification of Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones. J. Plant Res. 128:679–86
     [Google Scholar]
  22. 22.
    Choi J, Eom S, Shin K, Lee RA, Choi S et al. 2019. Identification of lysine histidine transporter 2 as an 1-aminocyclopropane carboxylic acid transporter in Arabidopsis thaliana by transgenic complementation approach. Front. Plant Sci. 10:1092
     [Google Scholar]
  23. 23.
    Cleland CF, Ajami A. 1974. Identification of the flower-inducing factor isolated from aphid honeydew as being salicylic acid. Plant Physiol. 54:904–6
     [Google Scholar]
  24. 24.
    Corratgé-Faillie C, Lacombe B. 2017. Substrate (un)specificity of Arabidopsis NRT1/PTR family (NPF) proteins. J. Exp. Bot. 68:123107–13
     [Google Scholar]
  25. 25.
    Daszkowska-Golec A. 2022. ABA is important not only under stress—revealed by the discovery of new ABA transporters. Trends Plant Sci. 27:423–25
     [Google Scholar]
  26. 26.
    David LC, Berquin P, Kanno Y, Seo M, Daniel-Vedele F, Ferrario-Méry S. 2016. N availability modulates the role of NPF3.1, a gibberellin transporter, in GA-mediated phenotypes in Arabidopsis. Planta 244:1315–28
     [Google Scholar]
  27. 27.
    Deslauriers SD, Spalding EP. 2021. Electrophysiological study of Arabidopsis ABCB4 and PIN2 auxin transporters: evidence of auxin activation and interaction enhancing auxin selectivity. Plant Direct 5:e361
     [Google Scholar]
  28. 28.
    Dietrich D, Pang L, Kobayashi A, Fozard JA, Boudolf V et al. 2017. Root hydrotropism is controlled via a cortex-specific growth mechanism. Nat. Plants 3:17057
     [Google Scholar]
  29. 29.
    Ding ZJ, Wang BJ, Moreno I, Dupláková N, Simon S et al. 2012. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 3:941
     [Google Scholar]
  30. 30.
    Do THT, Martinoia E, Lee Y. 2018. Functions of ABC transporters in plant growth and development. Curr. Opin. Plant Biol. 41:32–38
     [Google Scholar]
  31. 31.
    Do THT, Martinoia E, Lee Y, Hwang J-U. 2021. 2021 update on ATP-binding cassette (ABC) transporters: how they meet the needs of plants. Plant Physiol. 187:1876–92
     [Google Scholar]
  32. 32.
    Farquharson KL. 2012. An auxin influx transporter regulates vascular patterning in cotyledons. Plant Cell 24:2707
     [Google Scholar]
  33. 33.
    Feraru E, Feraru MI, Barbez E, Waidmann S, Sun L et al. 2019. PILS6 is a temperature-sensitive regulator of nuclear auxin input and organ growth in Arabidopsis thaliana. PNAS 9:3893–98Demonstrates that PILS6 controls cellular auxin sensitivity with high temperature–induced organ growth.
     [Google Scholar]
  34. 34.
    Fernie AR, Trethewey RN, Krotzky AJ, Willmitzer L. 2004. Metabolite profiling: from diagnostics to systems biology. Nat. Rev. Mol. 5:763–69
     [Google Scholar]
  35. 35.
    Friml J. 2022. Fourteen stations of auxin. Cold Spring Harb. Perspect. 14:a039859
     [Google Scholar]
  36. 36.
    Gasperini D, Chauvin A, Acosta IF, Kurenda A, Stolz S et al. 2015. Axial and radial oxylipin transport. Plant Physiol. 169:2244–54
     [Google Scholar]
  37. 37.
    Geisler M, Aryal B, Donato MD, Hao PC. 2017. A critical view on ABC transporters and their interacting partners in auxin transport. Plant Cell Physiol 58:101601–14
     [Google Scholar]
  38. 38.
    Geisler M, Wang B, Zhu J. 2013. Auxin transport during root gravitropism transporters and techniques. Plant Biol.50–57
     [Google Scholar]
  39. 39.
    Gillissen B, Burkle L, Andre B, Kuhn C, Rentsch D et al. 2000. A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell 12:2291–300
     [Google Scholar]
  40. 40.
    Gomi K. 2020. Jasmonic acid: an essential plant hormone. Int. J. Mol. Sci. 21:41261
     [Google Scholar]
  41. 41.
    Gräfe K, Schmitt L. 2020. The ABC transporter G subfamily in Arabidopsis thaliana. J. Exp. Bot. 72:192–106
     [Google Scholar]
  42. 42.
    Guan L, Denkert N, Eisa A, Lehmann M, Sjuts I et al. 2019. JASSY, a chloroplast outer membrane protein required for jasmonate biosynthesis. PNAS 116:10568–75Describes an outer chloroplast envelope–localized protein facilitating the export of OPDA.
     [Google Scholar]
  43. 43.
    Hammes UZ, Murphy AS, Schwechheimer C. 2022. Auxin transporters—a biochemical view. Cold Spring Harb. Perspect. 14:a039875
     [Google Scholar]
  44. 44.
    Han H, Adamowski M, Qi L, Alotaibi SS, Friml J. 2021. PIN-mediated polar auxin transport regulations in plant tropic responses. New Phytol. 232:510–22
     [Google Scholar]
  45. 45.
    Hartung W, Sauter A, Hose E. 2002. Abscisic acid in the xylem: Where does it come from, where does it go to?. J. Exp. Bot. 53:36627–32
     [Google Scholar]
  46. 46.
    Hedden P. 2020. The current status of research on gibberellin biosynthesis. Plant Cell Physiol. 61:1832–49
     [Google Scholar]
  47. 47.
    Hedden P, Kamiya Y. 1997. Gibberellin biosynthesis: enzymes, genes and their regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:431–60
     [Google Scholar]
  48. 48.
    Hedden P, Sponsel V. 2015. A century of gibberellin research. J. Plant Growth Regul. 34:740–60
     [Google Scholar]
  49. 49.
    Hejátko J, Hakoshima T, eds. 2018. Plant Structural Biology: Hormonal Regulations Cham, Switz.: Springer
  50. 50.
    Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M et al. 2006. Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–46
     [Google Scholar]
  51. 51.
    Hirose N, Makita N, Yamaya T, Sakakibara H. 2005. Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiol. 138:196–206
     [Google Scholar]
  52. 52.
    Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H. 2008. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 59:75–83
     [Google Scholar]
  53. 53.
    Hu Y, Omary M, Hu Y, Doron O, Hoermayer L et al. 2021. Cell kinetics of auxin transport and activity in Arabidopsis root growth and skewing. Nat. Commun. 12:1657
     [Google Scholar]
  54. 54.
    Hwang I, Sheen J, Muller B. 2012. Cytokinin signaling networks. Annu. Rev. Plant Biol. 63:353–80
     [Google Scholar]
  55. 55.
    Isoda R, Yoshinari A, Ishikawa Y, Sadoine M, Simon R et al. 2021. Sensors for the quantification localization and analysis of the dynamics of plant hormones. Plant J. 105:542–57
     [Google Scholar]
  56. 56.
    Jackson MB. 1993. Are plant hormones involved in root to shoot communication?. Adv. Bot. Res. 19:103–87
     [Google Scholar]
  57. 57.
    Jacobsen AGR, Jervis G, Xu J, Topping JF, Lindsey K. 2021. Root growth responses to mechanical impedance are regulated by a network of ROS, ethylene and auxin signaling in Arabidopsis. New Phytol. 231:225–42
     [Google Scholar]
  58. 58.
    Jenness MK, Carraro N, Pritchard CA, Murphy AS. 2019. The Arabidopsis ATP-BINDING CASSETTE transporter ABCB21 regulates auxin levels in cotyledons, the root pericycle, and leaves. Front. Plant Sci. 10:806
     [Google Scholar]
  59. 59.
    Jenness MK, Tayengwa R, Bate GA, Tapken W, Zhang YQ et al. 2022. Loss of multiple ABCB auxin transporters recapitulates the major twisted dwarf 1 phenotypes in Arabidopsis thaliana. Front. Plant Sci. 13:840260
     [Google Scholar]
  60. 60.
    Jenness MK, Tayengwa R, Murphy AS. 2020. An ATP-binding cassette transporter, ABCB19, regulates leaf position and morphology during phototropin1-mediated blue light responses. Plant Physiol. 184:1601–12
     [Google Scholar]
  61. 61.
    Jiang F, Hartung W. 2008. Long-distance signaling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J. Exp. Bot. 59:137–43
     [Google Scholar]
  62. 62.
    Jones AM, Danielson JÅH, ManojKumar SN, Lanquar V, Grossmann G, Frommer WB. 2014. Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. eLife 3:e01741
     [Google Scholar]
  63. 63.
    Jorgensen ME, Xu DY, Crocoll C, Ernst HA, Ramirez D et al. 2017. Origin and evolution of transporter substrate specificity within the NPF family. eLife 6:e19466
     [Google Scholar]
  64. 64.
    Kang J, Hwang J-U, Lee M, Kim Y-Y, Assmann SM et al. 2010. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. PNAS 107:2355–60Demonstrates that ABCG40 is an ABA importer regulating stomatal closure.
     [Google Scholar]
  65. 65.
    Kang J, Lee Y, Sakakibara H, Martinoia E. 2017. Cytokinin transporters: GO and STOP in signaling. Trends Plant Sci. 22:455–61
     [Google Scholar]
  66. 66.
    Kang J, Yim S, Choi H, Kim A, Lee KP et al. 2015. Abscisic acid transporters cooperate to control seed germination. Nat. Commun. 6:8113Shows that the ABA importers ABCG30 and ABCG40 and two ABA exporters, ABCG25 and ABCG31, regulate seed germination.
     [Google Scholar]
  67. 67.
    Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M et al. 2012. Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. PNAS 109:9653–58Identifies AIT1/NRT1.2 as an ABA importer regulating stomatal aperture in inflorescence stems.
     [Google Scholar]
  68. 68.
    Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T et al. 2016. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat. Commun. 7:13245Shows that AtSWEET13 and AtSWEET14 regulate GA transport and plant growth.
     [Google Scholar]
  69. 69.
    Kanstrup C, Nour-Eldin HH. 2022. The emerging role of the nitrate and peptide transporter family: NPF in plant specialized metabolism. Curr. Opin. Plant Biol. 68:102243
     [Google Scholar]
  70. 70.
    Khush GS. 1999. Green revolution: preparing for the 21st century. Genome 42:646–55
     [Google Scholar]
  71. 71.
    Kieber JJ. 2002. Tribute to Folke Skoog: recent advances in our understanding of cytokinin biology. J. Plant Growth Regul. 21:11–2
     [Google Scholar]
  72. 72.
    Kim A, Chen J, Khare D, Jin J-Y, Yamaoka Y et al. 2020. Non-intrinsic ATP-binding cassette proteins ABCI19, ABCI20 and ABCI21 modulate cytokinin response at the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell 39:473–87Demonstrates that ABCI19, ABCI20, and ABCI21 modulate cytokinin responses at the ER during early seedling development.
     [Google Scholar]
  73. 73.
    Ko D, Kang J, Kiba T, Park J, Kojima M et al. 2014. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. PNAS 111:7150–55Shows that ABCG14 regulates long-distance CK translocation from root to shoot through the vascular system.
     [Google Scholar]
  74. 74.
    Krattinger SG, Kang J, Bräunlich S, Boni R, Chauhan H et al. 2019. Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34. New Phytol. 223:853–66
     [Google Scholar]
  75. 75.
    Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18:927–37
     [Google Scholar]
  76. 76.
    Kudo T, Kiba T, Sakakibara H. 2010. Metabolism and long-distance translocation of cytokinins. J. Integr. Plant Biol. 52:153–60
     [Google Scholar]
  77. 77.
    Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E et al. 2010. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. PNAS 107:2361–66Shows that ABCG25 is a plasma membrane–localized ABA exporter regulating stomatal closure.
     [Google Scholar]
  78. 78.
    Kuromori T, Sugimoto E, Shinozaki K. 2014. Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Plant Physiol. 164:1587–92
     [Google Scholar]
  79. 79.
    Lacombe B, Achard P. 2016. Long-distance transport of phytohormones through the plant vascular system. Curr. Opin. Plant Biol. 34:1–8
     [Google Scholar]
  80. 80.
    Larsen B, Xu DY, Halkier BA, Nour-Eldin HH. 2017. Advances in methods for identification and characterization of plant transporter function. J. Exp. Bot. 68:154045–56
     [Google Scholar]
  81. 81.
    Lee KH, Piao HL, Kim HY, Choi SM, Jiang F et al. 2006. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–20
     [Google Scholar]
  82. 82.
    Léran S, Noguero M, Corratgé-Faillie C, Boursiac Y, Brachet C, Lacombe B. 2020. Functional characterization of the Arabidopsis abscisic acid transporters NPF4.5 and NPF4.6 in Xenopus oocytes. Front. Plant Sci. 11:144
     [Google Scholar]
  83. 83.
    Léran S, Varala K, Boyer J-C, Chiurazzi M, Crawford N et al. 2014. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci. 19:15–9
     [Google Scholar]
  84. 84.
    Li M, Wang F, Li S, Yu G, Wang L et al. 2020. Importers drive leaf-to-leaf jasmonic acid transmission in wound-induced systemic immunity. Mol. Plant 13:1485–98
     [Google Scholar]
  85. 85.
    Li M, Yu G, Cao C, Liu P. 2021. Metabolism, signaling, and transport of jasmonates. Plant Commun. 2:100231
     [Google Scholar]
  86. 86.
    Li Q, Zheng J, Li S, Huang G, Skilling SJ et al. 2017. Transporter-mediated nuclear entry of jasmonoyl-isoleucine is essential for jasmonate signaling. Mol. Plant 10:695–708
     [Google Scholar]
  87. 87.
    Liu P-P, Dahl CC, Park S-W, Klessig DF. 2011. Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and Tobacco. Plant Physiol. 155:1762–68
     [Google Scholar]
  88. 88.
    Longo A, Miles NW, Dickstein R. 2018. Genome mining of plant NPFs reveals varying conservation of signature motifs associated with the mechanism of transport. Front. Plant Sci. 9:1668
     [Google Scholar]
  89. 89.
    MacMillan J. 2001. Occurrence of gibberellins in vascular plants, fungi, and bacteria. J. Plant Growth Regul. 20:387–442
     [Google Scholar]
  90. 90.
    Mansfield TA, Schultes NP, Mourad GS. 2009. AtAzg1 and AtAzg2 comprise a novel family of purine transporters in Arabidopsis. FEBS Lett. 583:481–86
     [Google Scholar]
  91. 91.
    Manzi M, Lado J, Rodrigo MJ, Zacarías L, Arbona V, Gómez-Cadenas A. 2015. Root ABA accumulation in long-term water-stressed plants is sustained by hormone transport from aerial organs. Plant Cell Physiol. 56:2457–66
     [Google Scholar]
  92. 92.
    Matías-Hernández L, Aguilar-Jaramillo AE, Osnato M, Weistain R, Shani E et al. 2016. TEMPRANILLO reveals the mesophyll as crucial for epidermal trichome formation. Plant Physiol. 170:1624–39
     [Google Scholar]
  93. 93.
    Matosevich R, Cohen I, Gil-Yarom N, Modergo A, Friedlander-Shani L et al. 2020. Local auxin biosynthesis is required for root regeneration after wounding. Nat. Plants 6:1020–30
     [Google Scholar]
  94. 94.
    Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K et al. 2008. Cytokinins are central regulators of cambial activity. PNAS 105:5020027–31
     [Google Scholar]
  95. 95.
    McAdam SA, Brodribb TJ, Ross JJ. 2016. Shoot-derived abscisic acid promotes root growth. Plant Cell Environ. 39:652–59
     [Google Scholar]
  96. 96.
    McAdam SAM, Sussmilch FC, Brodribb TJ. 2016. Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant Cell Environ. 39:485–91
     [Google Scholar]
  97. 97.
    Mellor NL, Voß U, Janes G, Bennett MJ, Wells DM, Band LR. 2020. Auxin fluxes through plasmodesmata modify root-tip auxin distribution. Development 147:dev181669
     [Google Scholar]
  98. 98.
    Mellor NL, Voß U, Ware A, Janes G, Barrack D et al. 2022. Systems approaches reveal that ABCB and PIN proteins mediate co-dependent auxin efflux. Plant Cell 34:2309–27
     [Google Scholar]
  99. 99.
    Merchante C, Alonso JM, Stepanova AN. 2013. Ethylene signaling: simple ligand, complex regulation. Curr. Opin. Plant Biol. 16:554–60
     [Google Scholar]
  100. 100.
    Merilo E, Jalakas P, Laanemets K, Mohammadi O, Hõrak H et al. 2015. Abscisic acid transport and homeostasis in the context of stomatal regulation. Mol. Plant 8:1321–33
     [Google Scholar]
  101. 101.
    Michniewicz M, Ho C-H, Engers TA, Floro E, Damodaran S et al. 2019. TRANSPORTER OF IBA1 links auxin and cytokinin to influence root architecture. Dev. Cell 50:599–609.e4
     [Google Scholar]
  102. 102.
    Miller CO. 1961. A kinetin-like compound in maize. PNAS 47:2170–74
     [Google Scholar]
  103. 103.
    Morii M, Sugihara A, Takehara S, Kanno Y, Kawai K et al. 2020. The dual function of OsSWEET3a as a gibberellin and glucose transporter is important for young shoot development in rice. Plant Cell Physiol. 61:1935–45Shows that OsSWEET3a functions as both a sugar transporter and a GA transporter to regulate seed germination.
     [Google Scholar]
  104. 104.
    Morita M, Imanaka T. 2012. Peroxisomal ABC transporters: structure, function and role in disease. Biochim. Biophys. Acta. Mol. Basis Dis. 1822:1387–96
     [Google Scholar]
  105. 105.
    Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P et al. 2009. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–40
     [Google Scholar]
  106. 106.
    Munemasa S, Hauser F, Park J, Waadt R, Brandt B, Schroeder J. 2015. Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr. Opin. Plant Biol. 28:154–62
     [Google Scholar]
  107. 107.
    Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jorgensen ME et al. 2012. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488:531–34
     [Google Scholar]
  108. 108.
    Oslzewski N, Sun T-P, Gubler F. 2002. Gibberellin signaling biosynthesis, catabolism, and response pathways. Plant Cell 14:Suppl.S61–80
     [Google Scholar]
  109. 109.
    Osugi A, Mikiko K, Takebayashi Y, Ueda N, Kiba T, Sakakibara H. 2017. Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots. Nat. Plants 3:17112
     [Google Scholar]
  110. 110.
    Pandey BK, Huang GQ, Bhosale R, Hartman S, Sturrock CJ et al. 2021. Plant roots sense soil compaction through restricted ethylene diffusion. Science 371:276–80
     [Google Scholar]
  111. 111.
    Park J, Lee Y, Martinoia E, Geisler M. 2017. Plant hormone transporters: What we know and what we would like to know. BMC Biol. 15:93
     [Google Scholar]
  112. 112.
    Parker JL, Li C, Brinth A, Wang Z, Vogeley L, Solcan N et al. 2017. Proton movement and coupling in the POT family of peptide transporters. PNAS 114:13182–87
     [Google Scholar]
  113. 113.
    Paterlini A. 2020. Uncharted routes: exploring the relevance of auxin movement via plasmodesmata. Biol. Open 9:11bio055541
     [Google Scholar]
  114. 114.
    Pattyn J, Vaughan-Hirsch J, Van de Poel B. 2021. The regulation of ethylene biosynthesis: a complex multilevel control circuitry. New Phytol. 229:770–82
     [Google Scholar]
  115. 115.
    Pawela A, Banasiak J, Biała W, Martinoia E, Jasiński M. 2019. MtABCG20 is an ABA exporter influencing root morphology and seed germination of Medicago truncatula. Plant J. 98:511–23
     [Google Scholar]
  116. 116.
    Pingali PL. 2012. Green revolution: impacts, limits, and the path ahead. PNAS 109:3112302–8
     [Google Scholar]
  117. 117.
    Poel BV, Smet D, Straeten VD. 2015. Ethylene and hormone cross talk in vegetative growth and development. Plant Physiol. 169:61–72
     [Google Scholar]
  118. 118.
    Prigge MJ, Platre M, Kadakia N, Zhang Y, Greenham K et al. 2020. Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions. eLife 9:e54740
     [Google Scholar]
  119. 119.
    Qi ZY, Xiong LZ. 2013. Characterization of a purine permease family gene OsPUP7 involved in growth and development control in rice. J. Integr. Plant Biol. 55:111119–35
     [Google Scholar]
  120. 120.
    Qin P, Zhang G, Hu B, Wu J, Chen W et al. 2021. Leaf-derived ABA regulates rice seed development via a transporter-mediated and temperature-sensitive mechanism. Sci. Adv. 7:eabc8873Shows that rice DG1 regulates long-distance ABA transport and seed development.
     [Google Scholar]
  121. 121.
    Ranocha P, Dima O, Nagy R, Felten J, Corratgé-Faillie C et al. 2013. Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homeostasis. Nat. Commun. 4:2625
     [Google Scholar]
  122. 122.
    Rea PA. 2007. Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol. 58:347–75
     [Google Scholar]
  123. 123.
    Rees DC, Johnson E, Lewinson O 2009. ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 10:218–27
     [Google Scholar]
  124. 124.
    Retzer K, Akhmanova M, Konstantinova N, Malinska K, Leitner J et al. 2019. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nat. Commun. 10:5516
     [Google Scholar]
  125. 125.
    Rizza A, Jones AM. 2018. The makings of a gradient: spatiotemporal distribution of gibberellins in plant development. Curr. Opin. Plant Biol. 47:9–15
     [Google Scholar]
  126. 126.
    Rizza A, Tang B, Stanley CE, Grossmann G, Owen MR et al. 2021. Differential biosynthesis and cellular permeability explain longitudinal gibberellin gradients in growing roots. PNAS 118:8e1921960118
     [Google Scholar]
  127. 127.
    Rizza A, Walia A, Lanquar V, Frommer WB, Jones AM. 2017. In vivo gibberellin gradients visualized in rapidly elongating tissues. Nat. Plants 3:803–13
     [Google Scholar]
  128. 128.
    Rottmann TM, Fritz C, Lauter A, Schneider S, Fischer C et al. 2018. Protoplast-esculin assay as a new method to assay plant sucrose transporters: characterization of AtSUC6 and AtSUC7 sucrose uptake activity in Arabidopsis Col-0 ecotype. Front. Plant Sci. 9:430
     [Google Scholar]
  129. 129.
    Rowe JH, Jones AM. 2021. Focus on biosensors: looking through the lens of quantitative biology. Quant. Plant Biol. 2:e12
     [Google Scholar]
  130. 130.
    Saito H, Oikawa T, Hamamoto S, Ishimaru Y, Kanamori-Sato M et al. 2015. The jasmonate-responsive GTR1 transporter is required for gibberellin-mediated stamen development in Arabidopsis. Nat. Commun. 6:6095
     [Google Scholar]
  131. 131.
    Sakakibara H. 2021. Cytokinin biosynthesis and transport for systemic nitrogen signaling. Plant J. 105:421–30
     [Google Scholar]
  132. 132.
    Sato C, Aikawa K, Sugiyama S, Babeta K, Masuta C, Matsuura H. 2011. Distal transport of exogenously applied jasmonoyl-isoleucine with wounding stress. Plant Cell Physiol. 52:509–17
     [Google Scholar]
  133. 133.
    Sauer M, Kleine-Vehn J. 2019. PIN-FORMED and PIN-LIKES auxin transport facilitators. Development 146:dev168088
     [Google Scholar]
  134. 134.
    Sauter A, Davies WJ, Hartung W. 2001. The long-distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot. J. Exp. Bot. 52:3631991–97
     [Google Scholar]
  135. 135.
    Schulze A, Zimmer M, Kielke S, Stellmach H, Melnyk CW et al. 2019. Wound-induced shoot-to-root relocation of JA-Il2 precursors coordinates Arabidopsis growth. Mol. Plant 12:1383–94
     [Google Scholar]
  136. 136.
    Schwechheimer C. 2012. Gibberellin signaling in plants—the extended version. Front. Plant Sci. 2:107
     [Google Scholar]
  137. 137.
    Seltmann MA, Stingl NE, Lautenschlaeger JK, Krischke M. 2010. Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis. Plant Physiol. 152:1940–50
     [Google Scholar]
  138. 138.
    Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman J et al. 2009. The flowering hormone florigen functions as a general systemic regulator of growth and termination. PNAS 106:208392–97
     [Google Scholar]
  139. 139.
    Shi BH, Felipo-Benavent A, Cerutti G, Galvan-Ampudia G, Jilli L et al. 2022. A quantitative gibberellin signalling biosensor reveals a role for gibberellins in internode specification at the shoot apical meristem. bioRxiv 2021.06.11.448154. https://www.biorxiv.org/content/10.1101/2021.06.11.448154v2
  140. 140.
    Shimizu T, Kanno Y, Suzuki H, Watanabe S, Seo M. 2021. Arabidopsis NPF4.6 and NPF5.1 control leaf stomatal aperture by regulating abscisic acid transport. Genes 12:885
     [Google Scholar]
  141. 141.
    Shin K, Lee S, Song W-Y, Lee R-A, Lee I et al. 2015. Genetic identification of ACC-RESISTANT2 reveals involvement of lysine histidine TRANSPORTER1 in the uptake of 1-aminocyclopropane-1-carboxylic acid in Arabidopsis thaliana. Plant Cell Physiol. 56:572–82
     [Google Scholar]
  142. 142.
    Shohat H, Illouz-Eliaz N, Kanno Y, Seo M, Weiss D. 2020. The tomato DELLA protein PROCERA promotes abscisic acid responses in guard cells by upregulating an abscisic acid transporter. Plant Physiol. 184:518–28
     [Google Scholar]
  143. 143.
    Simon S, Skůpa P, Viaene T, Zwiewka M, Tejos R et al. 2016. PIN6 auxin transporter at endoplasmic reticulum and plasma membrane mediates auxin homeostasis and organogenesis in Arabidopsis. New Phytol. 211:65–74
     [Google Scholar]
  144. 144.
    Šimura J, Antoniadi I, Široká J, Tarkowská D, Strnad M et al. 2018. Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 177:476–89
     [Google Scholar]
  145. 145.
    Skalicky V, Kubes M, Napier R, Novak O. 2018. Auxins and cytokinins—the role of subcellular organization on homeostasis. Int. J. Mol. Sci. 19:103115
     [Google Scholar]
  146. 146.
    Su N, Zhu A, Tao X, Ding ZJ, Chang S et al. 2022. Structures and mechanisms of the Arabidopsis auxin transporter PIN3. Nature 609:616–21
     [Google Scholar]
  147. 147.
    Sun J, Hirose N, Wang X, Wen P, Xue L et al. 2005. Arabidopsis SOI33/AtENT8 gene encodes a putative equilibrative nucleoside transporter that is involved in cytokinin transport in planta. J. Integr. Plant Biol. 47:5588–603
     [Google Scholar]
  148. 148.
    Sun L, Feraru E, Feraru MI, Waidmann S, Wang WF et al. 2020. PIN-LIKES coordinate brassinosteroid signaling with nuclear auxin input in Arabidopsis thaliana. Curr. Biol. 30:1579–88.e6
     [Google Scholar]
  149. 149.
    Susila H, Jurić S, Liu L, Gawarecka K, Chung KS et al. 2021. Florigen sequestration in cellular membranes modulates temperature-responsive flowering. Science 373:1137–42
     [Google Scholar]
  150. 150.
    Swarup R, Peret B. 2012. AUX/LAX family of auxin influx carriers—an overview. Front. Plant Sci. 3:225
     [Google Scholar]
  151. 151.
    Takahashi F, Hanada K, Kondo T, Shinozaki K. 2019. Hormone-like peptides and small coding genes in plant stress signaling and development. Curr. Opin. Plant Biol. 51:88–95
     [Google Scholar]
  152. 152.
    Tal I, Zhang Y, Jørgensen ME, Pisanty O, Barbosa ICR et al. 2016. The Arabidopsis NPF3 protein is a GA transporter. Nat. Commun. 7:11486
     [Google Scholar]
  153. 153.
    Tan X, Li K, Wang Z, Zhu K, Tan X, Cao J. 2019. A review of plant vacuoles: formation, located proteins, and functions. Plants 8:9327
     [Google Scholar]
  154. 154.
    Tessi TM, Brumm S, Winklbauer E, Schumacher B, Pettinari G et al. 2021. Arabidopsis AZG2 transports cytokinins in vivo and regulates lateral root emergence. New Phytol. 229:979–93
     [Google Scholar]
  155. 155.
    Tessi TM, Shahriari M, Maurino VG, Meissner E, Novak O et al. 2020. The auxin transporter PIN1 and the cytokinin transporter AZG1 interact to regulate the root stress response. Curr. Biol. In press. https://doi.org/10.2139/ssrn.3733155
    [Google Scholar]
  156. 156.
    Theodoulou FL, Job K, Slocombe SP, Footitt S, Holdsworth M et al. 2005. Jasmonic acid levels are reduced in COMATOSE ATP-binding cassette transporter mutants. Implications for transport of jasmonate precursors into peroxisomes. Plant Physiol. 137:835–40
     [Google Scholar]
  157. 157.
    Thurow C, Krischke M, Mueller MJ, Gatz C. 2020. Induction of jasmonoyl-isoleucine (JA-Ile)-dependent JASMONATE ZIM-DOMAIN (JAZ) genes in NaCl-treated Arabidopsis thaliana roots can occur at very low JA-Ile levels and in the absence of the JA/JA-Ile transporter JAT1/AtABCG16. Plants 9:121635
     [Google Scholar]
  158. 158.
    Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K et al. 2007. Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–55
     [Google Scholar]
  159. 159.
    Ung KL, Winkler M, Schulz L, Kolb M, Janacek DP et al. 2022. Structures and mechanism of the plant PIN-FORMED auxin transporter. Nature 609:605–10
     [Google Scholar]
  160. 160.
    Verma C, Sawcjil MG, Linh NM, Scarpella E. 2015. Control of vein network topology by auxin transport. BMC Biol. 13:94
     [Google Scholar]
  161. 161.
    Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR et al. 2014. FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. eLife 3:e01739
     [Google Scholar]
  162. 162.
    Wang J, Song L, Gong X, Xu J, Li M. 2020. Functions of jasmonic acid in plant regulation and response to abiotic stress. Int. J. Mol. Sci. 21:41446
     [Google Scholar]
  163. 163.
    Wang S, Alseekh S, Fernie AR, Luo J. 2009. The structure and function of major plant metabolite modifications. Mol. Plant 12:899–919
     [Google Scholar]
  164. 164.
    Wasternack C, Hause B. 2018. A bypass in jasmonate biosynthesis—the OPR3—independent formation. Trends Plant Sci. 23:4276–79
     [Google Scholar]
  165. 165.
    Watanabe S, Takahashi N, Kanno Y, Suzuki H, Aoi Y et al. 2020. The Arabidopsis NRT1/PTR FAMILY protein NPF7.3/NRT1.5 is an indole-3-butyric acid transporter involved in root gravitropism. PNAS 117:4931500–9
     [Google Scholar]
  166. 166.
    Wilkinson S, Davies WJ. 2002. ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ. 25:195–210
     [Google Scholar]
  167. 167.
    Winnicki K, Polit JT, Zabka A, Maszewski J. 2021. Do plasmodesmata play a prominent role in regulation of auxin-dependent genes at early stages of embryogenesis?. Cells 10:733
     [Google Scholar]
  168. 168.
    Wu GS, Carville JS, Spalding EP. 2016. ABCB19-mediated polar auxin transport modulates Arabidopsis hypocotyl elongation and the endoreplication variant of the cell cycle. Plant J. 85:209–18
     [Google Scholar]
  169. 169.
    Wulff N, Ernst HA, Jorgensen ME, Lambertz S, Maierhofer T et al. 2019. An optimized screen reduces the number of GA transporters and provides insights into nitrate transporter 1/peptide transporter family substrate determinants. Front. Plant Sci. 10:1106
     [Google Scholar]
  170. 170.
    Xiao Y, Liu D, Zhang G, Gao S, Liu L et al. 2019. Big Grain3, encoding a purine permease, regulates grain size via modulating cytokinin transport in rice. J. Integr. Plant Biol. 61:5581–97
     [Google Scholar]
  171. 171.
    Xu Z-Y, Lee KH, Dong T, Jeong JC, Jin JB et al. 2012. A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:52184–99
     [Google Scholar]
  172. 172.
    Xuan W, De Gernier H, Beeckman T. 2020. The dynamic nature and regulation of the root clock. Development 147:3dev181446
     [Google Scholar]
  173. 173.
    Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59:225–51
     [Google Scholar]
  174. 174.
    Yang Z, Xia J, Hong J, Zhang C, Wei H et al. 2022. Structural insights into auxin recognition and efflux by Arabidopsis PIN1. Nature 609:611–15
     [Google Scholar]
  175. 175.
    Yao L, Cheng X, Gu Z, Huang W, Li S et al. 2018. The AWPM-19 family protein OsPM1 mediates abscisic acid influx and drought response in rice. Plant Cell 30:1258–76
     [Google Scholar]
  176. 176.
    Zeevaart JAD, Creelman RA. 1988. Metabolism and physiology of abscisic acid. . Annu. Rev. Plant Physiol. Plant Mol. Biol. 39:439–73
     [Google Scholar]
  177. 177.
    Zhang CH, Hicks GR, Raikhel NV. 2015. Molecular composition of plant vacuoles: important but less understood regulations and roles of tonoplast lipids. Plants 4:320–33
     [Google Scholar]
  178. 178.
    Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L. 2014. A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol. Plant 7:1522–32
     [Google Scholar]
  179. 179.
    Zhang K, Novak O, Wei Z, Gou M, Zhang X et al. 2014. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat. Commun. 5:3274
     [Google Scholar]
  180. 180.
    Zhang Y, Nasser V, Pisanty O, Omary M, Wulff N et al. 2018. A transportome-scale amiRNA-based screen identifies redundant roles of Arabidopsis ABCB6 and ABCB20 in auxin transport. Nat. Commun. 9:4204Uses a multitargeted artificial microRNA approach to overcome redundancy and identify hormone transport mechanisms.
     [Google Scholar]
  181. 181.
    Zhang Y, Vasuki H, Liu J, Bar H, Lazary S et al. 2021. ABA homeostasis and long-distance translocation are redundantly regulated by ABCG ABA importers. Sci. Adv. 7:43eabf6069Shows that ABCG17 and ABCG18 ABA importers regulate stomata aperture and long-distance ABA.
     [Google Scholar]
  182. 182.
    Zhao J, Ding BL, Zhu E, Deng XJ, Zhang MY et al. 2021. Phloem unloading via the apoplastic pathway is essential for shoot distribution of root-synthesized cytokinin. Plant Physiol. 186:2111–23
     [Google Scholar]
  183. 183.
    Zhao J, Yu N, Ju M, Fan B, Zhang Y et al. 2019. ABC transporter OsABCG18 controls the shootward transport of cytokinins and grain yield in rice. J. Exp. Bot. 70:6277–91
     [Google Scholar]
  184. 184.
    Zhao X, Li N, Song Q, Li X, Meng H, Luo K. 2021. OPDAT1, a plastid envelope protein involved in 12-oxo-phytodienoic acid export for jasmonic acid biosynthesis in Populus. Tree Physiol. 41:1714–28
     [Google Scholar]
  185. 185.
    Zhou Y, Wang Y, Li J, Liang J. 2021. In vivo FRET–FLIM reveals ER-specific increases in the ABA level upon environmental stresses. Plant Physiol. 186:1545–61
     [Google Scholar]
  186. 186.
    Zourelidou M, Absmanner B, Weller B, Barbosa ICR, Willige BC et al. 2014. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3:e02860
     [Google Scholar]
  187. 187.
    Zurcher E, Liu JC, Donato MD, Geisler M, Muller B. 2016. Plant development regulated by cytokinin sinks. Science 353:63031027–30
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-070722-015329
Loading
Plant Hormone Transport and Localization: Signaling Molecules on the Move
Annual Review of Plant Biology 74, 453 (2023); https://doi.org/10.1146/annurev-arplant-070722-015329
/content/journals/10.1146/annurev-arplant-070722-015329
/content/journals/10.1146/annurev-arplant-070722-015329
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

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