1932

Abstract

Hydathodes are organs found on aerial parts of a wide range of plant species that provide almost direct access for several pathogenic microbes to the plant vascular system. Hydathodes are better known as the site of guttation, which is the release of droplets of plant apoplastic fluid to the outer leaf surface. Because these organs are only described through sporadic allusions in the literature, this review aims to provide a comprehensive view of hydathode development, physiology, and immunity by compiling a historic and contemporary bibliography. In particular, we refine the definition of hydathodes.We illustrate their important roles in the maintenance of plant osmotic balance, nutrient retrieval, and exclusion of deleterious chemicals from the xylem sap. Finally, we present our current understanding of the infection of hydathodes by adapted vascular pathogens and the associated plant immune responses.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-082718-100228
2019-08-25
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/phyto/57/1/annurev-phyto-082718-100228.html?itemId=/content/journals/10.1146/annurev-phyto-082718-100228&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abley K, Sauret-Güeto S, Marée AF, Coen E 2016. Formation of polarity convergences underlying shoot outgrowths. eLife 5:e18165
    [Google Scholar]
  2. 2. 
    Agrios GN. 2005. Plant Pathology Cambridge, MA: Acad. Press, 5th ed..
    [Google Scholar]
  3. 3. 
    Aloni R. 1995. The induction of vascular tissues by auxin and cytokinin. Plant Hormones531–46 Dordrecht, Neth.: Springer
    [Google Scholar]
  4. 4. 
    Aloni R. 2001. Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J. Plant Growth Regul. 20:22–34
    [Google Scholar]
  5. 5. 
    Aloni R, Schwalm K, Langhans M, Ullrich CI 2003. Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–53
    [Google Scholar]
  6. 6. 
    Alvarez JP, Furumizu C, Efroni I, Eshed Y, Bowman JL 2016. Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife 5:e15023
    [Google Scholar]
  7. 7. 
    Alvarez JP, Goldshmidt A, Efroni I, Bowman JL, Eshed Y 2009. The NGATHA distal organ development genes are essential for style specification in Arabidopsis. Plant Cell 21:1373–93
    [Google Scholar]
  8. 8. 
    Ascensão L, Mota L, de Moraes Castro M 1999. Glandular trichomes on the leaves and flowers of Plectranthus ornatus: morphology, distribution and histochemistry. Ann. Bot. 84:437–47
    [Google Scholar]
  9. 9. 
    Bailey KJ, Leegood RC. 2016. Nitrogen recycling from the xylem in rice leaves: dependence upon metabolism and associated changes in xylem hydraulics. J. Exp. Bot. 67:2901–11
    [Google Scholar]
  10. 10. 
    Baylis T, Cierlik I, Sundberg E, Mattsson J 2013. SHORT INTERNODES/STYLISH genes, regulators of auxin biosynthesis, are involved in leaf vein development in Arabidopsis thaliana. New Phytol 197:737–50
    [Google Scholar]
  11. 11. 
    Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A et al. 2014. Expression patterns of flagellin sensing 2 map to bacterial entry sites in plant shoots and roots. J. Exp. Bot. 65:6487–98
    [Google Scholar]
  12. 12. 
    Belin-Depoux M. 1989. Des hydathodes aux nectaires foliaires chez les plantes tropicales. Bull. Soc. Bot. France Actual. Bot. 136:151–68
    [Google Scholar]
  13. 13. 
    Bergmann D. 2006. Stomatal development: from neighborly to global communication. Curr. Opin. Plant Biol. 9:478–83
    [Google Scholar]
  14. 14. 
    Biles CL, Abeles FB. 1991. Xylem sap proteins. Plant Physiol 96:597–601
    [Google Scholar]
  15. 15. 
    Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A et al. 2011. Model for the regulation of Arabidopsis thaliana leaf margin development. PNAS 108:3424–29
    [Google Scholar]
  16. 16. 
    Biot E, Cortizo M, Burguet J, Kiss A, Oughou M et al. 2016. Multiscale quantification of morphodynamics: MorphoLeaf, software for 2-D shape analysis. Development 143:183417–28
    [Google Scholar]
  17. 17. 
    Bittel P, Robatzek S. 2007. Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr. Opin. Plant Biol. 10:4335–41
    [Google Scholar]
  18. 18. 
    Burgerstein A. 1904. Die Transpiration der Pflanzen Jena, Ger.: Gustav Fischer
    [Google Scholar]
  19. 19. 
    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]
  20. 20. 
    Büttner D, Bonas U. 2010. Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol. Rev. 34:107–33
    [Google Scholar]
  21. 21. 
    Carlton WM, Braun EJ, Gleason ML 1998. Ingress of Clavibactermichiganensis subsp. michiganensis into tomato leaves through hydathodes. Phytopathology 88:525–9
    [Google Scholar]
  22. 22. 
    Cerutti A, Jauneau A, Auriac M-C, Lauber E, Martinez Y et al. 2017. Immunity at cauliflower hydathodes controls infection by Xanthomonas campestris pv. campestris. Plant Physiol 174:2700–16Arabidopsis water pores can respond to the abiotic environment.
    [Google Scholar]
  23. 23. 
    Chater CCC, Caine RS, Fleming AJ, Gray JE 2017. Origins and evolution of stomatal development. Plant Physiol 174:624–38
    [Google Scholar]
  24. 24. 
    Chen C-C, Chen Y-R. 2005. Study on laminar hydathodes of Ficus formosana (Moraceae) I. Morphology and ultrastructure. Bot. Bull. Acad. Sin. 46:205–15
    [Google Scholar]
  25. 25. 
    Chen C-C, Chen Y-R. 2006. Study on laminar hydathodes of Ficus formosana (Moraceae) II. Morphogenesis of hydathodes. Bot. Stud. 47:279–92
    [Google Scholar]
  26. 26. 
    Chen C-C, Chen Y-R. 2007. Study on laminar hydathodes of Ficus formosana (Moraceae) III. Salt injury of guttation on hydathodes. Bot. Stud. 48:215–26
    [Google Scholar]
  27. 27. 
    Chen C-C, Chen Y-R. 2016. Study on the laminar hydathodes of Ficus formosana (Moraceae) IV. Coated vesicles endocytosis is one of the retrieval mechanisms of epithem during guttation. Taiwania 61:194–200
    [Google Scholar]
  28. 28. 
    Chen Y-C, Lin T-C, Martin CE 2014. Effects of guttation prevention on photosynthesis and transpiration in leaves of Alchemilla mollis. Photosynthetica 52:371–76
    [Google Scholar]
  29. 29. 
    Colmenero-Flores JM, Martínez G, Gamba G, Vázquez N, Iglesias DJ et al. 2007. Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50:278–92
    [Google Scholar]
  30. 30. 
    Curtis JD, Lersten NR. 1986. Hydathode anatomy in Potentilla palustris (Rosaceae). Nord. J. Bot. 6:793–96
    [Google Scholar]
  31. 31. 
    Curtis LC. 1943. Deleterious effects of guttation fluids on foliage. Am. J. Bot. 30:778–82
    [Google Scholar]
  32. 32. 
    Dieffenbach H, Kramer D, Lüttge U 1980. Release of guttation fluid from passive hydathodes of intact barley plants. I. Structural and cytological aspects. Ann. Bot. 45:397–401
    [Google Scholar]
  33. 33. 
    Drennan PM, Goldsworthy D, Buswell A 2009. Marginal and laminar hydathode-like structures in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. Flora Morphol. Distrib. Funct. Ecol. Plants 204:210–19
    [Google Scholar]
  34. 34. 
    Eklund DM, Ståldal V, Valsecchi I, Cierlik I, Eriksson C et al. 2010. The Arabidopsis thaliana STYLISH1 protein acts as a transcriptional activator regulating auxin biosynthesis. Plant Cell 22:349–63
    [Google Scholar]
  35. 35. 
    Elias TS, Gelband H. 1977. Morphology, anatomy, and relationship of extrafloral nectaries and hydathodes in two species of Impatiens (Balsaminaceae). Bot. Gaz. 138:206–12
    [Google Scholar]
  36. 36. 
    Endo RM, Oertli JJ. 1964. Stimulation of fungal infection of Bentgrass. Nature 201:313
    [Google Scholar]
  37. 37. 
    Fahn A. 1988. Secretory tissues in vascular plants. New Phytol 108:229–57
    [Google Scholar]
  38. 38. 
    Feild TS, Arens NC. 2007. The ecophysiology of early angiosperms. Plant Cell Environ 30:291–309
    [Google Scholar]
  39. 39. 
    Feild TS, Sage TL, Czerniak C, Iles WJD 2005. Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation-induced flooding of the mesophyll. Plant Cell Environ 28:1179–90
    [Google Scholar]
  40. 40. 
    Feng T, Kuo T. 1975. Bacterial leaf blight of rice plant. VI. Chemotactic responses of Xanthomonas oryzae to water droplets exudated from water pores on the leaf of rice plants. Bot. Bull. Acad. Sin. 16:126–36
    [Google Scholar]
  41. 41. 
    Fukui R, Fukui H, Alvarez AM 1999. Suppression of bacterial blight by a bacterial community isolated from the guttation fluids of anthuriums. Appl. Environ. Microbiol. 65:1020–28
    [Google Scholar]
  42. 42. 
    Fukui R, Fukui H, McElhaney R, Nelson SC, Alvarez AM 1996. Relationship between symptom development and actual sites of infection in leaves of Anthurium inoculated with a bioluminescent strain of Xanthomonas campestris pv. dieffenbachiae. Appl. Environ. Microbiol. 62:1021–28
    [Google Scholar]
  43. 43. 
    Fukushima K, Hasebe M. 2014. Adaxial–abaxial polarity: the developmental basis of leaf shape diversity. Genesis 52:1–18
    [Google Scholar]
  44. 44. 
    Galatis B. 1988. Microtubules and epithem-cell morphogenesis in hydathodes of Pilea cadierei. Planta 176:287–97
    [Google Scholar]
  45. 45. 
    Gardner MJ, Baker AJ, Assie JM, Poethig RS, Haseloff JP, Webb AAR 2009. GAL4 GFP enhancer trap lines for analysis of stomatal guard cell development and gene expression. J. Exp. Bot. 60:213–26
    [Google Scholar]
  46. 46. 
    Gay PA, Tuzun S. 2000. Involvement of a novel peroxidase isozyme and lignification in hydathodes in resistance to black rot disease in cabbage. Can. J. Bot. 78:1144–49
    [Google Scholar]
  47. 47. 
    Geisler M, Nadeau J, Sack FD 2000. Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–86
    [Google Scholar]
  48. 48. 
    Goatley JL, Lewis RW. 1966. Composition of guttation fluid from rye, wheat, and barley seedlings. Plant Physiol 41:373–75
    [Google Scholar]
  49. 49. 
    Goursat M-J, Guignard J-L. 1970. De la présence d'hydathodes dans le coléoptile d'Hordeum vulgare L. Bull. Soc. Bot. France 117:243–46
    [Google Scholar]
  50. 50. 
    Govier RN, Brown JGS, Pate JS 1968. Hemiparasitic nutrition in angiosperms. II. Root haustoria and leaf glands of Odontites verna (Bell.) Dum. and their relevance to the abstraction of solutes from the host. New Phytol 67:963–72
    [Google Scholar]
  51. 51. 
    Grunwald I, Rupprecht I, Schuster G, Kloppstech K 2003. Identification of guttation fluid proteins: the presence of pathogenesis-related proteins in non-infected barley plants. Physiol. Plant. 119:192–202
    [Google Scholar]
  52. 52. 
    Gu G, Cevallos-Cevallos JM, van Bruggen AHC 2013. Ingress of Salmonella enterica Typhimurium into tomato leaves through hydathodes. PLOS ONE 8:e53470
    [Google Scholar]
  53. 53. 
    Gudesblat GE, Torres PS, Vojnov AA 2009. Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149:1017–27
    [Google Scholar]
  54. 54. 
    Guo A, Leach JE. 1989. Examination of rice hydathode water pores exposed to Xanthomonas campestris pv. oryzae. Phytopathology 79:433–36
    [Google Scholar]
  55. 55. 
    Haberlandt G. 1914. Physiological Plant Anatomy London: MacmillanIn this cornerstone book, the author clearly defines epithemal hydathodes.
    [Google Scholar]
  56. 56. 
    Hacquard S, Spaepen S, Garrido-Oter R, Schulze-Lefert P 2017. Interplay between innate immunity and the plant microbiota. Annu. Rev. Phytopathol. 55:565–89
    [Google Scholar]
  57. 57. 
    Ham JH, Majerczak DR, Arroyo-Rodriguez AS, Mackey DM, Coplin DL 2006. WtsE, an AvrE-family effector protein from Pantoea stewartii subsp. stewartii, causes disease-associated cell death in corn and requires a chaperone protein for stability. Mol. Plant-Microbe Interact. 19:1092–102
    [Google Scholar]
  58. 58. 
    Harrison PM, Arosio P. 1996. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275:161–203
    [Google Scholar]
  59. 59. 
    Hay A, Barkoulas M, Tsiantis M 2006. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133:3955–61
    [Google Scholar]
  60. 60. 
    Heinrich G. 1973. Die feinstruktur der trichom-hydathoden von Monarda fistulosa. Protoplasma 77:271–78
    [Google Scholar]
  61. 61. 
    Heisler MG, Ohno C, Das P, Sieber P, Reddy GV et al. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15:1899–911
    [Google Scholar]
  62. 62. 
    Hong J, Peralta-Videa JR, Rico C, Sahi S, Viveros MN et al. 2014. Evidence of translocation and physiological impacts of foliar applied CeO2 nanoparticles on cucumber (Cucumis sativus) plants. Environ. Sci. Technol. 48:4376–85
    [Google Scholar]
  63. 63. 
    Horino O. 1984. Ultrastructure of water pores in Leersia japonica Makino and Oryza sativa L.: its correlation with the resistance to hydathodal invasion of Xanthomonas campestris pv. oryzae. Jpn. J. Phytopathol. 50:72–76
    [Google Scholar]
  64. 64. 
    Hou S, Wang X, Chen D, Yang X, Wang M et al. 2014. The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7. PLOS Pathog 10:e1004331
    [Google Scholar]
  65. 65. 
    Hugouvieux V, Barber CE, Daniels MJ 1998. Entry of Xanthomonas campestris pv. campestris into hydathodes of Arabidopsis thaliana leaves: a system for studying early infection events in bacterial pathogenesis. Mol. Plant-Microbe Interact. 11:537–43
    [Google Scholar]
  66. 66. 
    Islam MN, Kawasaki M. 2015. Evaluation of calcium regulating roles of guttation and calcium oxalate crystals in leaf blades and petioles of hydroponically grown eddo. Plant Prod. Sci. 18:11–21
    [Google Scholar]
  67. 67. 
    Johnson MA 1937. Hydathodes in the genus Equisetum. Bot. Gaz 98:598–608
    [Google Scholar]
  68. 68. 
    Kawamura E, Horiguchi G, Tsukaya H 2010. Mechanisms of leaf tooth formation in Arabidopsis. Plant J 62:429–41
    [Google Scholar]
  69. 69. 
    Kim SJ, Kim KW, Cho MH, Franceschi VR, Davin LB, Lewis NG 2007. Expression of cinnamyl alcohol dehydrogenases and their putative homologues during Arabidopsis thaliana growth and development: lessons for database annotations?. Phytochemistry 68:1957–74
    [Google Scholar]
  70. 70. 
    Kiran R, Singh PP 2015. Effect of rain simulation on Xanthomonas oryzae pv. oryzae population density in guttation fluid and on the spread of bacterial blight in rice. J. Appl. Natural Sci. 7:72–76
    [Google Scholar]
  71. 71. 
    Klepper B, Kaufmann MR 1966. Removal of salt from xylem sap by leaves and stems of guttating plants. Plant Physiol 41:1743–47
    [Google Scholar]
  72. 72. 
    Kondo Y, Tamaki T, Fukuda H 2014. Regulation of xylem cell fate. Front. Plant Sci. 5:315
    [Google Scholar]
  73. 73. 
    Kumar Verma R, Samal B, Chatterjee S 2018. Xanthomonas oryzae pv. oryzae chemotaxis components and chemoreceptor Mcp2 are involved in the sensing of constituents of xylem sap and contribute to the regulation of virulence-associated functions and entry into rice. Mol. Plant Pathol. 19:112397–415Chemotaxis is important for infection of rice hydathodes by Xoo.
    [Google Scholar]
  74. 74. 
    Kwon C, Neu C, Pajonk S, Yun HS, Lipka U et al. 2008. Co-option of a default secretory pathway for plant immune responses. Nature 451:835–40
    [Google Scholar]
  75. 75. 
    Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F et al. 1996. Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J 9:195–203
    [Google Scholar]
  76. 76. 
    Le J, Liu X-G, Yang K-Z, Chen X-L, Zou J-J et al. 2014. Auxin transport and activity regulate stomatal patterning and development. Nat. Commun. 5:3090
    [Google Scholar]
  77. 77. 
    Lee RC, Burton RA, Hrmova M, Fincher GB 2001. Barley arabinoxylan arabinofuranohydrolases: purification, characterization and determination of primary structures from cDNA clones. Biochem. J. 356:181–89
    [Google Scholar]
  78. 78. 
    Leme FM, Scremin-Dias E 2014. Ecological interpretations of the leaf anatomy of amphibious species of Aeschynomene L. (Leguminosae–Papilionoideae). Brazilian J. Biol. 74:41–51
    [Google Scholar]
  79. 79. 
    Lepeschkin WW 1923. Über aktive und passive Wasserdrüsen und Wasserspalten. Plant Biol 41:298–300
    [Google Scholar]
  80. 80. 
    Lersten NR, Curtis JD 1982. Hydathodes in Physocarpus (Rosaceae: Spiraeoideae). Can. J. Bot. 60:850–85
    [Google Scholar]
  81. 81. 
    Lersten NR, Curtis JD 1985. Distribution and anatomy of hydathodes in Asteraceae. Bot. Gaz 146:106–14
    [Google Scholar]
  82. 82. 
    Lersten NR, Curtis JD 1991. Laminar hydathodes in Urticaceae: survey of tribes and anatomical observations on Pilea pumila and Urtica dioica. Plant Syst. Evol 176:179–203
    [Google Scholar]
  83. 83. 
    Lersten NR, Peterson WH 1974. Anatomy of hydathodes and pigment disks in leaves of Ficus diversifolia (Moraceae). Bot. J. Linn. Soc. 68:109–13
    [Google Scholar]
  84. 84. 
    Lewis RW. 1962. Guttation fluid: effects on growth of Claviceps purpurea in vitro. Science 138:690–91
    [Google Scholar]
  85. 85. 
    Macho AP, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54:2263–72
    [Google Scholar]
  86. 86. 
    Maeda E, Maeda K. 1988. Ultrastructural studies of leaf hydathodes. Jpn. J. Crop Sci. 57:733–42
    [Google Scholar]
  87. 87. 
    Martin CE, Von Willert DJ 2000. Leaf epidermal hydathodes and the ecophysiological consequences of foliar water uptake in species of Crassula from the Namib Desert in southern Africa. Plant Biol 2:229–42
    [Google Scholar]
  88. 88. 
    Martínez-Fernández I, Sanchís S, Marini N, Balanzá V, Ballester P et al. 2014. The effect of NGATHA altered activity on auxin signaling pathways within the Arabidopsis gynoecium. Front. Plant Sci 5:210
    [Google Scholar]
  89. 89. 
    Mattson MP, Chan SL. 2003. Calcium orchestrates apoptosis. Nat. Cell Biol. 5:1041–43
    [Google Scholar]
  90. 90. 
    Maugarny-Cales A, Laufs P. 2018. Getting leaves into shape: a molecular, cellular, environmental and evolutionary view. Development 145:dev161646
    [Google Scholar]
  91. 91. 
    Melotto M, Underwood W, Koczan J, Nomura K, He SY 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80
    [Google Scholar]
  92. 92. 
    Melotto M, Zhang L, Oblessuc PR, He SY 2017. Stomatal defense a decade later. Plant Physiol 174:561–71
    [Google Scholar]
  93. 93. 
    Merelo P, Paredes EB, Heisler MG, Wenkel S 2017. The shady side of leaf development: the role of the REVOLUTA/KANADI1 module in leaf patterning and auxin-mediated growth promotion. Curr. Opin. Plant Biol. 35:111–16
    [Google Scholar]
  94. 94. 
    Merilo E, Yarmolinsky D, Jalakas P, Parik H, Tulva I et al. 2018. Stomatal VPD response: There is more to the story than ABA. Plant Physiol 176:851–64
    [Google Scholar]
  95. 95. 
    Metcalfe CR, Chalk L. 1979. Anatomy of the Dicotyledons Oxford, UK: Clarendon Press
    [Google Scholar]
  96. 96. 
    Mew TW, Mew I-pC, Huang JS 1984. Scanning electron microscopy of virulent and avirulent strains of Xanthomonas campestris pv. oryzae on rice leaves. Phytopathology 74:635–41
    [Google Scholar]
  97. 97. 
    Miotto-Vilanova L, Jacquard C, Courteaux B, Wortham L, Michel J et al. 2016. Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front. Plant Sci. 7:1236
    [Google Scholar]
  98. 98. 
    Mizuno N, Takahashi A, Wagatsuma T, Mizuno T, Obata H 2002. Chemical composition of guttation fluid and leaves of Petasites japonicus v. giganteus and Polygonum cuspidatum growing on ultramafic soil. Soil Sci. Plant Nutr. 48:451–53
    [Google Scholar]
  99. 99. 
    Morales J, Kadota Y, Zipfel C, Molina A, Torres MA 2016. The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J. Exp. Bot. 67:1663–76
    [Google Scholar]
  100. 100. 
    Mortlock C. 1952. The structure and development of the hydathodes of Ranunculus fluitans Lam. New Phytol 51:129–38
    [Google Scholar]
  101. 101. 
    Munting A. 1672. Waare oeffening der Planten Amsterdam: Voor Jan Rieuwertsz
    [Google Scholar]
  102. 102. 
    Nadeau JA, Sack FD. 2002. Stomatal development in Arabidopsis. Arabidopsis Book 1:e0066
    [Google Scholar]
  103. 103. 
    Nagai M, Ohnishi M, Uehara T, Yamagami M, Miura E et al. 2013. Ion gradients in xylem exudate and guttation fluid related to tissue ion levels along primary leaves of barley. Plant Cell Environ 36:1826–37
    [Google Scholar]
  104. 104. 
    Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K 2012. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell Online 24:519–35The PRESSED FLOWER and WOX1 genes that define the middle domain in leaves are required for the formation of hydathodes on the Arabidopsis leaf margin.
    [Google Scholar]
  105. 105. 
    Nazoa P, Vidmar JJ, Tranbarger TJ, Mouline K, Damiani I et al. 2003. Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol. Biol. 52:689–703
    [Google Scholar]
  106. 106. 
    Nguyen CT, Agorio A, Jossier M, Depré S, Thomine S, Filleur S 2016. Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol 57:764–75
    [Google Scholar]
  107. 107. 
    Niño-Liu DO, Ronald PC, Bogdanove AJ 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol. Plant Pathol. 7:5303–24
    [Google Scholar]
  108. 108. 
    Palzkill DA, Tibbitts TW. 1977. Evidence that root pressure flow is required for calcium transport to head leaves of cabbage. Plant Physiol 60:854–56
    [Google Scholar]
  109. 109. 
    Pantin F, Renaud J, Barbier F, Vavasseur A, Le Thiec D et al. 2013. Developmental priming of stomatal sensitivity to abscisic acid by leaf microclimate. Curr. Biol. 23:1805–11
    [Google Scholar]
  110. 110. 
    Papanatsiou M, Amtmann A, Blatt MR 2016. Stomatal spacing safeguards stomatal dynamics by facilitating guard cell ion transport independent of the epidermal solute reservoir. Plant Physiol 172:254–63
    [Google Scholar]
  111. 111. 
    Payne WW. 1979. Stomatal patterns in embryophytes: their evolution, ontogeny and interpretation. Taxon 28:117–32
    [Google Scholar]
  112. 112. 
    Pedersen O. 1993. Long-distance water transport in aquatic plants. Plant Physiol 103:1369–75
    [Google Scholar]
  113. 113. 
    Pedersen O, Bolt Jørgensen L, Sand-Jensen K 1997. Through-flow of water in leaves of a submerged plant is influenced by the apical opening. Planta 202:43–50
    [Google Scholar]
  114. 114. 
    Penfield S, Clements S, Bailey KJ, Gilday AD, Leegood RC et al. 2012. Expression and manipulation of PHOSPHOENOLPYRUVATE CARBOXYKINASE 1 identifies a role for malate metabolism in stomatal closure. Plant J 69:679–88
    [Google Scholar]
  115. 115. 
    Perrin A. 1970. Diversité des formes d'accumulation de la phytoferritine dans les cellules constituant l'épithème des hydathodes de Taraxacum officinale. Weber et Saxifraga aizoon Jacq. Planta 93:71–81
    [Google Scholar]
  116. 116. 
    Perrin A. 1972. Contribution à l'étude de l'organisation et du fonctionnement des hydathodes: recherches anatomiques ultrastructurales et physiologiques. PhD Thesis Univ. Lyon France:Provides a synthesis of the hydathode literature before the decline of this research field in the 1980s.
    [Google Scholar]
  117. 117. 
    Perrin A. 1972. Organisation et nature de l'inclusion cristalline des organites du type “crystal-containing body” rencontrés dans les cellules de l'épithéme des hydathodes de Cichorium intybus L. et Taraxacum officinale Weber. Protoplasma 74:213–25
    [Google Scholar]
  118. 118. 
    Persson M, Staal J, Oide S, Dixelius C 2009. Layers of defense responses to Leptosphaeria maculans below the RLM1- and camalexin-dependent resistances. New Phytol 182:470–82
    [Google Scholar]
  119. 119. 
    Pillitteri LJ, Bogenschutz NL, Torii KU 2008. The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis. Plant Cell Physiol 49:934–43
    [Google Scholar]
  120. 120. 
    Pillitteri LJ, Dong J. 2013. Stomatal development in Arabidopsis. Arabidopsis Book 11:e0162
    [Google Scholar]
  121. 121. 
    Pillitteri LJ, Torii KU. 2012. Mechanisms of stomatal development. Annu. Rev. Plant Biol. 63:591–614
    [Google Scholar]
  122. 122. 
    Pilot G, Gaymard F, Mouline K, Chérel I, Sentenac H 2003. Regulated expression of Arabidopsis Shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol. Biol. 51:773–87
    [Google Scholar]
  123. 123. 
    Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U et al. 2004. Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. Plant Cell 16:1827–40
    [Google Scholar]
  124. 124. 
    Poethig RS. 1997. Leaf morphogenesis in flowering plants. Plant Cell 9:1077–87
    [Google Scholar]
  125. 125. 
    Pratelli R, Voll LM, Horst RJ, Frommer WB, Pilot G 2010. Stimulation of nonselective amino acid export by glutamine dumper proteins. Plant Physiol 152:762–73
    [Google Scholar]
  126. 126. 
    Preston GM. 2000. Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol. Plant Pathol. 1:263–75
    [Google Scholar]
  127. 127. 
    Reams WM. 1953. The occurrence and ontogeny of hydathodes in Hygrophila polysperma T. Anders. New Phytol 52:8–13
    [Google Scholar]
  128. 128. 
    Robène-Soustrade I, Laurent P, Gagnevin L, Jouen E, Pruvost O 2006. Specific detection of Xanthomonas axonopodis pv. dieffenbachiae in Anthurium (Anthurium andreanum) tissues by nested PCR. Appl. Environ. Microbiol. 72:1072–78
    [Google Scholar]
  129. 129. 
    Rundel PW. 1982. Water uptake by organs other than roots. Physiological Plant Ecology II OL Lange, PS Nobel, CB Osmond, H Ziegler 111–34 Berlin: Springer–Verlag
    [Google Scholar]
  130. 130. 
    Sachs T. 1991. Pattern Formation in Plant Tissues New York: Cambridge Univ. Press
    [Google Scholar]
  131. 131. 
    Samac DA, Shah DM. 1991. Developmental and pathogen-induced activation of the Arabidopsis acidic chitinase promoter. Plant Cell 3:1063–72
    [Google Scholar]
  132. 132. 
    Scarpella E, Marcos D, Friml J, Berleth T 2006. Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–27
    [Google Scholar]
  133. 133. 
    Schaller J, Brackhage C, Paasch S, Brunner E, Bäucker E, Dudel EG 2013. Silica uptake from nanoparticles and silica condensation state in different tissues of Phragmites australis. Sci. Total Environ 442:6–9
    [Google Scholar]
  134. 134. 
    Schneider H, Thürmer F, Zhu JJ, Wistuba N, Gessner P et al. 1999. Diurnal changes in xylem pressure of the hydrated resurrection plant Myrothamnus flabellifolia: evidence for lipid bodies in conducting xylem vessels. New Phytol 143:471–84
    [Google Scholar]
  135. 135. 
    Schofield RA, Bi Y-M, Kant S, Rothstein SJ 2009. Over-expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant Cell Environ 32:271–85
    [Google Scholar]
  136. 136. 
    Schulze W, Weise A, Frommer WB, Ward JM 2000. Function of the cytosolic N-terminus of sucrose transporter AtSUT2 in substrate affinity. FEBS Lett 485:189–94
    [Google Scholar]
  137. 137. 
    Schwartz AR, Morbitzer R, Lahaye T, Staskawicz BJ 2017. TALE-induced bHLH transcription factors that activate a pectate lyase contribute to water soaking in bacterial spot of tomato. PNAS 114:E897–903
    [Google Scholar]
  138. 138. 
    Serrano M, Coluccia F, Torres M, L'Haridon F, Métraux J-P 2014. The cuticle and plant defense to pathogens. Front. Plant Sci. 5:274
    [Google Scholar]
  139. 139. 
    Shapira O, Israeli Y, Shani U, Schwartz A 2013. Salt stress aggravates boron toxicity symptoms in banana leaves by impairing guttation. Plant Cell Environ 36:275–87
    [Google Scholar]
  140. 140. 
    Sharabani G, Manulis-Sasson S, Borenstein M, Shulhani R, Lofthouse M et al. 2013. The significance of guttation in the secondary spread of Clavibacter michiganensis subsp. michiganensis in tomato greenhouses. Plant Pathol 62:578–86
    [Google Scholar]
  141. 141. 
    Shatil-Cohen A, Moshelion M. 2012. Smart pipes: the bundle sheath role as xylem-mesophyll barrier. Plant Signal. Behav. 7:1088–91A joint action of the bundle sheath and guttation through hydathodes protects the mesophyll from flooding.
    [Google Scholar]
  142. 142. 
    Sheldrake AR. 1973. Do coleoptile tips produce auxin?. New Phytol 72:433–47
    [Google Scholar]
  143. 143. 
    Sheldrake AR, Northcote DH. 1968. Some constituents of xylem sap and their possible relationship to xylem differentiation. J. Exp. Bot. 19:681–89
    [Google Scholar]
  144. 144. 
    Shibagaki N, Rose A, Jeffrey PM, Fujiwara T, Hayashi H et al. 2002. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–86
    [Google Scholar]
  145. 145. 
    Singh S, Singh TN 2013. Guttation 1: chemistry, crop husbandry and molecular farming. Phytochem. Rev 12:147–72
    [Google Scholar]
  146. 146. 
    Sperry JS. 1983. Observations on the structure and function of hydathodes in Blechnum lehmannii. Am. Fern J 73:65–72
    [Google Scholar]
  147. 147. 
    Stevens ABP. 1956. The structure and development of the hydathodes of Caltha palustris L. New Phytol 55:339–45
    [Google Scholar]
  148. 148. 
    Stevens CJ, Wilson J, McAllister HA 2012. Biological flora of the British Isles: Campanula rotundifolia. J. Ecol. 100:821–39
    [Google Scholar]
  149. 149. 
    Stocking CR. 1956. Guttation and bleeding. Pflanze und Wasser/Water Relations of Plants489–502 Berlin: Springer
    [Google Scholar]
  150. 150. 
    Sutton T, Baumann U, Hayes J, Collins NC, Shi B-J et al. 2007. Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–49
    [Google Scholar]
  151. 151. 
    Světlíková P, Hájek T, Těšitel J 2015. Hydathode trichomes actively secreting water from leaves play a key role in the physiology and evolution of root-parasitic rhinanthoid Orobanchaceae. Ann. Bot. 116:61–68
    [Google Scholar]
  152. 152. 
    Tadege M, Lin H, Bedair M, Berbel A, Wen J et al. 2011. STENOFOLIA regulates blade outgrowth and leaf vascular patterning in Medicago truncatula and Nicotiana sylvestris. Plant Cell 23:2125–42
    [Google Scholar]
  153. 153. 
    Takeda F, Wisniewski ME, Glenn DM 1991. Occlusion of water pores prevents guttation in older strawberry leaves. J. Am. Soc. Horticult. Sci. 116:1122–25
    [Google Scholar]
  154. 154. 
    Tancos MA, Chalupowicz L, Barash I, Manulis-Sasson S, Smart CD 2013. Tomato fruit and seed colonization by Clavibacter michiganensis subsp. michiganensis through external and internal routes. Appl. Environ. Microbiol. 79:6948–57
    [Google Scholar]
  155. 155. 
    Tanner W, Beevers H. 2001. Transpiration, a prerequisite for long-distance transport of minerals in plants?. PNAS 98:9443–47
    [Google Scholar]
  156. 156. 
    Těšitel J, Tesařová M. 2013. Ultrastructure of hydathode trichomes of hemiparasitic Rhinanthus alectorolophus and Odontites vernus: How important is their role in physiology and evolution of parasitism in Orobanchaceae?. Plant Biol 15:119–25
    [Google Scholar]
  157. 157. 
    Thompson AJ, Andrews J, Mulholland BJ, McKee JM, Hilton HW et al. 2007. Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143:1905–17
    [Google Scholar]
  158. 158. 
    Thomson WW. 1975. The Structure and Function of Salt Glands Berlin: Springer
    [Google Scholar]
  159. 159. 
    Timmons SA, Posluszny U, Gerrath JM 2007. Morphological and anatomical development in the Vitaceae. X. Comparative ontogeny and phylogenetic implications of Cissus quadrangularis L. Can. J. Bot. 85:860–72
    [Google Scholar]
  160. 160. 
    Tsukaya H, Shoda K, Kim GT, Uchimiya H 2000. Heteroblasty in Arabidopsis thaliana (L.) Heynh. Planta 210:536–42
    [Google Scholar]
  161. 161. 
    Tucker SC, Hoefert LL. 1968. Ontogeny of the tendril in Vitis vinifera. Am. J. Bot 55:1110–19
    [Google Scholar]
  162. 162. 
    Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T 2009. Differential recruitment of WOX transcription factors for lateral development and organ fusion in petunia and Arabidopsis. Plant Cell Online 21:2269–83
    [Google Scholar]
  163. 163. 
    Wan J, Tanaka K, Zhang X-C, Son GH, Brechenmacher L et al. 2012. LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 160:396–406
    [Google Scholar]
  164. 164. 
    Wang W, Xu B, Wang H, Li J, Huang H, Xu L 2011. YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol 157:1805–19Multiple yucca mutant phenotypes show that hydathode formation in Arabidopsis requires local auxin production.
    [Google Scholar]
  165. 165. 
    Wang Y, Ribot C, Rezzonico E, Poirier Y 2004. Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135:400–11
    [Google Scholar]
  166. 166. 
    Weintraub RL, Miller WE, Schantz EJ 1958. Chemical stimulation of germination of spores of Piricularia oryzae. Phytopathology 48:7–10
    [Google Scholar]
  167. 167. 
    Wightman R, Wallis S, Aston P 2018. Leaf margin organisation and the existence of vaterite-producing hydathodes in the alpine plant Saxifraga scardica. Flora 241:27–34
    [Google Scholar]
  168. 168. 
    Wilkinson HP. 2007. Leaf teeth in certain Salicaceae and ‘Flacourtiaceae’. Bot. J. Linn. Soc. 155:241–56
    [Google Scholar]
  169. 169. 
    Williams PH. 1980. Black rot: a continuing threat to world crucifers. Plant Disease 64:736–42
    [Google Scholar]
  170. 170. 
    Wilson JK. 1923. The nature and reaction of water from hydathodes Bull., Cornell Agric. Exp. Stn. Ithaca, NY:
    [Google Scholar]
  171. 171. 
    Wu Y, Xun Q, Guo Y, Zhang J, Cheng K et al. 2016. Genome-wide expression pattern analyses of the Arabidopsis leucine-rich repeat receptor-like kinases. Mol. Plant 9:289–300
    [Google Scholar]
  172. 172. 
    Xin X-F, Nomura K, Aung K, Velásquez AC, Yao J et al. 2016. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539:524–29
    [Google Scholar]
  173. 173. 
    Yadeta KA, Thomma BPHJ. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 4:97
    [Google Scholar]
  174. 174. 
    Yamaguchi T, Nukazuka A, Tsukaya H 2012. Leaf adaxial-abaxial polarity specification and lamina outgrowth: evolution and development. Plant Cell Physiol 53:1180–94
    [Google Scholar]
  175. 175. 
    Yamaji N, Mitatni N, Ma JF 2008. A transporter regulating silicon distribution in rice shoots. Plant Cell 20:1381–89
    [Google Scholar]
  176. 176. 
    Ye Y, Yuan J, Chang X, Yang M, Zhang L et al. 2015. The phosphate transporter gene OsPht1;4 is involved in phosphate homeostasis in rice. PLOS ONE 10:e0126186
    [Google Scholar]
  177. 177. 
    Ye Z-H. 2002. Vascular tissue differentiation and pattern formation in plants. Annu. Rev. Plant Biol. 53:183–202
    [Google Scholar]
  178. 178. 
    Young SA, Guo A, Guikema JA, White FF, Leach JE 1995. Rice cationic peroxidase accumulates in xylem vessels during incompatible interactions with Xanthomonas oryzae pv oryzae. Plant Physiol 107:1333–41
    [Google Scholar]
  179. 179. 
    Yu A, Lepere G, Jay F, Wang J, Bapaume L et al. 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS 110:2389–94
    [Google Scholar]
  180. 180. 
    Yu S, Pratelli R, Denbow C, Pilot G 2015. Suppressor mutations in the Glutamine Dumper1 protein dissociate disturbance in amino acid transport from other characteristics of the Gdu1D phenotype. Front. Plant Sci. 6:593
    [Google Scholar]
  181. 181. 
    Yuan F, Leng B, Wang B 2016. Progress in studying salt secretion from the salt slands in recretohalophytes: How do plants secrete salt?. Front. Plant Sci. 7:977
    [Google Scholar]
  182. 182. 
    Zgurski JM. 2005. Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis leaves. Plant Cell 17:77–91
    [Google Scholar]
  183. 183. 
    Zhang H, He X, Zhang Z, Zhang P, Li Y et al. 2011. Nano-CeO2 exhibits adverse effects at environmental relevant concentrations. Environ. Sci. Technol. 45:3725–30
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-082718-100228
Loading
/content/journals/10.1146/annurev-phyto-082718-100228
Loading

Data & Media loading...

Supplementary Data

  • 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