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Guttation: Quantification, Microbiology and Implications for Phytopathology

  • Sanjay SinghEmail author
Chapter
Part of the Progress in Botany book series (BOTANY, volume 75)

Abstract

Guttation is the process of liquid exudation from hydathodes situated on the tip, along the margins and adaxial and abaxial surfaces of leaves. Hydathodes, also known as water stomata or water pores, unlike stomata, are always open representing the path of least resistance to the liquid outflow from them. Guttation fluids contain a variety of living and non-living ingredients. The living materials include algae, fungi, bacteria, viroids and viruses. The non-living organic constituents include toxins, mycotoxins, alkaloids, proteins, enzymes, sugars, amino acids, volatiles, hormones, vitamins, etc., and the inorganic components include Na, K, Ca, Mg, Mn, B, Co, Zn, Se, Ni, Fl, Si, As, Al, Cl, NH4, NO3, PO4, SO4, CO3, HCO3, etc. This review highlights various techniques for measuring guttation, both qualitative and quantitative, and their use and utility are discussed. Further, the microbiological aspects of guttation, with particular reference to the incidence of algal, fungal, bacterial and viral diseases and toxins produced by these pathogenic organisms, are described. The production of new chemicals by host plant as strategies to protect from harmful effects of pathogens is also outlined. The goal here is to stimulate discussion on our gaps of knowledge in the physiology and biochemistry related to guttation including genetic aspects, and the microbiology associated with guttation. A long-range goal is to design and create improved plant types with increased productivity, and developing effective control measures for plant diseases, to help sustain agriculture in a world with a burgeoning human population. A better understanding of the physiology behind guttation might contribute substantially to this aspiration.

Keywords

Endophytic Fungus Root Pressure Brome Mosaic Virus Rice Yellow Mottle Virus Guttation Fluid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The author expresses his sincere gratitude to Prof. Ulrich Luettge, Institut fuer Botanik,Technische Universitaet, Darmstadt, Germany, and Editor-in-Chief of ‘Progress in Botany’ for having invited to write this review paper as well as for his fatherly affection during the preparation of the manuscript. The author also extends thanks to Prof. Kym F. Faull, University of California, Los Angeles, USA, for critically reading the manuscript. Dr. Amare Ayalew, Head, School of Plant Sciences, Prof. Chemeda Fininsa, Academic Vice-President, and Dr. Nigussie Dechassa, Research Vice-President of Haramaya University, Ethiopia, also deserve thanks for their sustained cooperation and guidance during the preparation of the manuscript.

References

  1. Adler CL, Lock JA, Fleet RW (2008) Rainbows in the grass. II. Arbitrary diagonal incidence. Appl Opt 47:214–219CrossRefGoogle Scholar
  2. Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56:1535–1544PubMedCrossRefGoogle Scholar
  3. Bald JG (1952) Stomatal droplets and the penetration of leaves by plant pathogens. Am J Bot 39:97–99CrossRefGoogle Scholar
  4. Brandl MT, Amundson R (2008) Leaf age as a risk factor in contamination of lettuce with Escherichia coli O157:H7 and Salmonella enterica. Appl Environ Microbiol 74:2298–2306PubMedCrossRefGoogle Scholar
  5. Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194PubMedCrossRefGoogle Scholar
  6. Cantrill LC, Overall RL, Goodwin PB (1999) Cell-to-cell communication via plant endomembranes. Cell Biol Int 23:653–661PubMedCrossRefGoogle Scholar
  7. Carlton WM, Braun EJ, Gleason ML (1998) Ingress of Clavibacter michiganensis subsp. Michiganensis into tomato leaves through hydathodes. Phytopathology 88:525–529PubMedCrossRefGoogle Scholar
  8. Chen C-C, Chen Y-R (2005) Study on laminar hydathodes of Ficus formosana (Moraceae) I. morphology and ultrastructure. Bot Bull Acad Sin 46:205–215Google Scholar
  9. Chen C-C, Chen Y-R (2006) Study on laminar hydathodes of Ficus formosana (Moraceae). II. Morphogenesis of hydathodes. Bot Stud 47:279–292Google Scholar
  10. Chen C-C, Chen Y-R (2007) Study on laminar hydathodes of Ficus formosana (moraceae) III. Salt injury of guttation on hydathodes. Bot Stud 48:215–226Google Scholar
  11. Crawford KM, Zambryski PC (1999) Plasmodesmata signaling: many roles, sophisticated statutes. Curr Opin Plant Biol 2:382–387PubMedCrossRefGoogle Scholar
  12. Curtis LC (1943) Deleterious effects of guttated fluids on foliage. Am J Bot 30:778–781CrossRefGoogle Scholar
  13. Daniell H, Khan MS, Allison L (2002) Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. Trends Plant Sci 7:84–91PubMedCrossRefGoogle Scholar
  14. Dieffenbach H, Kramer D, Luttge U (1980a) Release of guttation fluid from passive hydathodes of intact barley plants. I. Structural and cytological aspects. Ann Bot 45:397–401Google Scholar
  15. Dieffenbach H, Lüttge U, Pitman MG (1980b) Release of guttation fluid from passive hydathodes of intact barley plants. II. The effects of abscisic acid and cytokinins. Ann Bot 45:703–712Google Scholar
  16. Ding XS, Boydston CM, Nelson RS (2001) Presence of Brome mosaic virus in barley guttation fluid and its association with localized cell death response. Phytopathology 91:440–448PubMedCrossRefGoogle Scholar
  17. Dustmamatov AG, Zholkevish VN, Kuznetsov VV (2004) Water pumping activity of the root system in the process of cross-adaptation of sunflower plants to hyperthermia and water deficiency. Russ J Plant Physiol 51:822–826CrossRefGoogle Scholar
  18. Endo RM (1967) The role of guttation fluid in fungal disease development. Calif Turfgrass Cult 17:12–13Google Scholar
  19. Fletcher AT, Mader JC (2007) Hormone profiling by LC-QToF-MS/MS in dormant Macadamia integrifolia: correlations with abnormal vertical growth. Plant Growth Regul 26:351–361CrossRefGoogle Scholar
  20. French CJ, Elder M (1999) Virus particles in guttate and xylem of infected cucumber (Cucumis sativus L.). Ann Appl Biol 134:81–87CrossRefGoogle Scholar
  21. French CJ, Elder M, Skelton F (1993) Recovering and identifying infectious plant viruses in guttation fluid. HortScience 28:746–747Google Scholar
  22. Frisvad JC, Smedsgaard J, Larsen TO, Samson RA (2004) Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol 49:201–241Google Scholar
  23. Fukui H, Fukui R, Alvarez AM (1996) Role of indigenous leaf-inhabiting bacteria in suppression of anthurium blight. Phytopathology 86:S36–S36Google Scholar
  24. 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 65:1020–1028PubMedGoogle Scholar
  25. Galan JE, Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567–573PubMedCrossRefGoogle Scholar
  26. Gareis M, Gareis E (2007) Guttation droplets of Penicillium nordicum and Penicillium verrucosum contain high concentrations of the mycotoxins ochratoxin A and B. Mycopathologia 163:207–214PubMedCrossRefGoogle Scholar
  27. 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 78:1144–1149Google Scholar
  28. Georgiou CD, Patsoukis N, Papapostolou I, Zervoudakis G (2006) Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr Comp Biol 46:691–712PubMedCrossRefGoogle Scholar
  29. Goatley JL, Lewis RW (1966) Composition of guttation fluid from rye, wheat, and barley seedlings. Plant Physiol 41:373–375PubMedCrossRefGoogle Scholar
  30. Gophna U, Ron EZ, Graur D (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312:151–163PubMedCrossRefGoogle Scholar
  31. Grovel O, Pouchus YF, Verbist JF (2003) Accumulation of gliotoxin, a cytotoxic mycotoxin from Aspergillus fumigatus, in blue mussel (Mytilus edulis). Toxicon 42:297–300PubMedCrossRefGoogle Scholar
  32. 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 119:192–202CrossRefGoogle Scholar
  33. Guiry MD, Guiry GM (2008) Vaucheria. Algae base. World-wide electronic publication, National University of Ireland, GalwayGoogle Scholar
  34. Hughes RN, Brimblecombe P (1994) Dew and guttation: formation and environmental significance in agricultural and forest meteorology. Agric For Meteorol 67:173–190CrossRefGoogle Scholar
  35. 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 11:537–543PubMedCrossRefGoogle Scholar
  36. Hutwimmer S, Wang H, Strasser H, Burgstaller W (2010) Formation of exudate droplets by Metarhizium anisopliae and the presence of destruxins. Mycologia 102:1–10PubMedCrossRefGoogle Scholar
  37. Ivanoff SS (1963) Guttation injuries of plants. Bot Rev 29:202–229CrossRefGoogle Scholar
  38. Jackson RW (2009) Plant pathogenic bacteria: genomics and molecular biology. Horizon Scientific Press, NorwichGoogle Scholar
  39. Jennings DH (1991) The role of droplets in helping to maintain a constant growth rate of aerial hyphae. Mycol Res 95:883–884CrossRefGoogle Scholar
  40. Johnson J (1936) Relation of root pressure to plant disease. Science 84:135–136PubMedCrossRefGoogle Scholar
  41. Kerstetter RE, Zepp RG, Carreira LH (1998) Peroxidases in grass dew derived from guttation: possible role in polymerization of soil organic matter. Biogeochemistry 42:311–323CrossRefGoogle Scholar
  42. Komarnytsky S, Borisjuk NV, Borisjuk LG, Alam MZ, Raskin I (2000) Production of recombinant proteins in tobacco guttation fluid. Plant Physiol 124:927–934PubMedCrossRefGoogle Scholar
  43. Koulman A, Lane GA, Christensen MJ, Fraser K, Tapper BA (2007) Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 68:355–360PubMedCrossRefGoogle Scholar
  44. Koulman A, Lee TV, Fraser K, Johnson L, Arcus V, Lott JS, Rasmussen S, Lane G (2012) Identification of extracellular siderophores and a related peptide from the endophytic fungus Epichloe festucae in culture and endophyte-infected Lolium perenne. Phytochemistry 75:128–139PubMedCrossRefGoogle Scholar
  45. Krasnoff SB, Keresztes I, Gillilan RE, Szebenyi DME, Donzelli BGG, Churchill ACL, Gibson DM (2007) Serinocyclins A and B, cyclic heptapeptides from Metarhizium anisopliae. J Natl Prod 70:1919–1924CrossRefGoogle Scholar
  46. Lee RE (2008) Phycology, 4th edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  47. Lersten LR, Curtis JD (1982) Hydathodes in Physocarpus (Rosaceae: Spiraeoideae). Can J Bot 60:850–855CrossRefGoogle Scholar
  48. Lersten LR, Curtis JD (1985) Distribution and anatomy of hydathodes in Asteraceae. Bot Gaz 146:106–114CrossRefGoogle Scholar
  49. Lersten LR, Curtis JD (1991) Laminar hydathodes in Urticaceae: survey of tribes and anatomical observation on Pilea pumila and Urtica dioica. Plant Syst Evol 176:179–203CrossRefGoogle Scholar
  50. Lewis RW (1962) Guttation fluid: effects on growth of Claviceps purpurea in vitro. Science 138:690–691PubMedCrossRefGoogle Scholar
  51. Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol 25:910–920CrossRefGoogle Scholar
  52. Lock JA, Adler CL, Fleet RW (2008) Rainbows in the grass. I. External-reflection rainbows from pendant droplets. Appl Opt 47:203–213CrossRefGoogle Scholar
  53. Logvenkov SA (1993a) On the guttation mechanism in plants. Biophysics 38:865–869Google Scholar
  54. Logvenkov SA (1993b) The guttation mechanism in plants. Biophysics 38:889–894Google Scholar
  55. Luo W, Goudriaan J (2000) Dew formation on rice under varying durations of nocturnal radiative loss. Agric For Meteorol 104:303–313CrossRefGoogle Scholar
  56. Maeda E, Maeda K (1987) Ultrastructural studies of leaf hydathodes. I. Wheat (Triticum aestivum) leaf tips. Jpn J Crop Sci 56:641–651CrossRefGoogle Scholar
  57. Maeda E, Maeda K (1988) Ultrastructural studies of leaf hydathodes II. Rice (Oryza sativa) leaf tips. Jpn J Crop Sci 57:733–742CrossRefGoogle Scholar
  58. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  59. Munnecke DE, Chandler PA (1957) A leaf spot of Philodendron related to stomatal exudation and to temperature. Phytopathology 47:299–303Google Scholar
  60. Noda T, Kaku H (1999) Growth of Xanthomonas oryzae pv. oryzae in planta and in guttation fluid of rice. Ann Phytopathol Soc Jpn 65:9–14CrossRefGoogle Scholar
  61. Pedersen O (1993) Long-distance water transport in aquatic plants. Plant Physiol 103:1369–1375PubMedGoogle Scholar
  62. Pedersen O (1994) Acropetal water transport in submerged plants. Bot Acta l07:61–65Google Scholar
  63. Pedersen O, Jurgensen LB, Sand-Jensen K (1997) Through-flow of water in leaves of a submerged plant is influenced by the apical opening. Planta 202:43–50CrossRefGoogle Scholar
  64. Peterson KM, Rychel AL, Torii KU (2010) Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22:296–306PubMedCrossRefGoogle Scholar
  65. Pillitteri LJ, Bogenschutz NL, Torii KU (2008) The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis. Plant Cell Physiol 49:934–943PubMedCrossRefGoogle Scholar
  66. Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U, Wingate VP, Frommer WB (2004) Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. Plant Cell 16:1827–1840PubMedCrossRefGoogle Scholar
  67. Raleigh GJ (1946) The effect of various ions on guttation of the tomato. Plant Physiol 2:194–200CrossRefGoogle Scholar
  68. Rao YP, Srivastava DN (1970) Application of phages in investigation of epidemiology of bacterial blight disease of rice. Proc Indian Natl Sci Acad 37:314–321Google Scholar
  69. Raper KB, Thom C (1949) A manual of the Penicillia. Williams and Wilkins, Baltimore, MDGoogle Scholar
  70. Raper KB, Thom C (1968) A manual of the Penicillia. Hafner Publishing Company, New YorkGoogle Scholar
  71. Richards K (2004) Observation and simulation of dew in rural and urban environments. Progr Phys Geogr 28:76–94CrossRefGoogle Scholar
  72. Romantschuk M (1992) Attachment of plant pathogenic bacteria to plant surfaces. Annu Rev Phytopathol 30:225–243PubMedCrossRefGoogle Scholar
  73. Ryan RP, Vorholter F-J, Potnis N, Jones JB, Van Sluys M-A, Bogdanove AJ, Dow JM (2011) Pathogenomics of Xanthomonas: understanding bacterium–plant interactions. Nat Rev Microbiol 9:344–355PubMedCrossRefGoogle Scholar
  74. Rybicki EP (2009) Third international conference on plant-based vaccines and antibodies. Expert Rev Vaccines 8:1151–1155PubMedCrossRefGoogle Scholar
  75. Samson RA, Gams W (1984) The taxonomic situation in the hyphomycete genera Penicillium, Aspergillus and Fusarium. Antonie Van Leeuwenhoek 50:815–824PubMedCrossRefGoogle Scholar
  76. Schmidt O, Czeschlik D (2006) Wood and tree fungi. Springer, BerlinGoogle Scholar
  77. Schoelz JE, Harries PA, Nelson RS (2011) Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant 4(5):813–831. doi: 10.1093/mp/ssr070 PubMedCrossRefGoogle Scholar
  78. Scott J, Untereiner WA, Wong B, Straus NA, Malloch D (2004) Genotypic variation in Penicillium chysogenum from indoor environments. Mycologia 96:1095–1105PubMedCrossRefGoogle Scholar
  79. Sharabani G, Manulis-Sasson S, Borenstein M, Shulhani R, Lofthouse M, Chalupowicz L, Shtienberg D (2012) The significance of guttation in the secondary spread of Clavibacter michiganensis subsp. michiganensis in tomato greenhouses. Plant Pathol 62(3):578–586. doi: 10.1111/j.1365-3059.2012.02673.x CrossRefGoogle Scholar
  80. Shepherd RW, Wagner GJ (2007) Phylloplane proteins: emerging defences at the aerial frontline? Trends Plant Sci 12:51–56PubMedCrossRefGoogle Scholar
  81. Singh S, Singh TN (2013) Guttation 1: chemistry, crop husbandry and molecular farming. Phytochem Rev 12:147–172. doi: 10.1007/s11101-012-9269-x CrossRefGoogle Scholar
  82. Singh S, Chauhan JS, Singh TN (2008) Guttation: a potential yield enhancing trait in rice. Curr Sci 95:455–456Google Scholar
  83. Singh S, Singh TN, Chauhan JS (2009) Guttation in rice: occurrence, regulation, and significance in varietal improvement. J Crop Improv 23:351–365CrossRefGoogle Scholar
  84. Slewinski TL, Meeley R, Braun DM (2009) Sucrose transporter1 functions in phloem loading in maize leaves. J Exp Bot 60:881–892PubMedCrossRefGoogle Scholar
  85. Smith EF (1898) Some bacterial diseases of truck crops. Transactions of the Peninsula Horticultural Society, XI annual session, pp 142–147Google Scholar
  86. Smith MN, Olien CR (1978) Pathological factors affecting survival of winter barley following controlled freeze tests. Phytopathology 68:773–777CrossRefGoogle Scholar
  87. Southworth D (2012) Biocomplexity of plant-fungal interactions. Wiley, Hoboken, NJCrossRefGoogle Scholar
  88. Sperry JS (1983) Observations on the structure and function of hydathodes in Blechnum lehmannii. Am Fern J 73:65–72CrossRefGoogle Scholar
  89. Stocking CR (1956) Guttation and bleeding. In: Ruhland W (ed) Encyclopedia of plant physiology, vol III. Springer, Berlin, pp 489–502Google Scholar
  90. Sutton T, Baumann U, Hayes J, Collins NC, Shi B-J, Schnurbusch T, Hay A, Mayo G, Pallotta M, Tester M, Langridge P (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449PubMedCrossRefGoogle Scholar
  91. Takeda F, Glenn DM (1989) Hydathode anatomy and the relationship between guttation and plant water status in strawberry (Fragaria x ananassa duch.). Acta Hortic (ISHS) 265:387–392Google Scholar
  92. Traore MD, Traore VSE, Galzi-Pinel A, Fargette D, Konate G, Traore AS, Traore O (2008) Abiotic transmission of rice yellow mottle virus through soil and contact between plants. Pak J Biol Sci 11:900–904PubMedCrossRefGoogle Scholar
  93. Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93:3–11PubMedCrossRefGoogle Scholar
  94. Wang C, Skrobek A, Butt TM (2004) Investigations on the destruxin production of the entomopathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 85:168–174PubMedCrossRefGoogle Scholar
  95. Wang W, Ben X, Wang H, Li J, Huang H et al (2011) YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol 157:1805–1819PubMedCrossRefGoogle Scholar
  96. Yao J, Allen C (2006) Chemotaxis is required for virulence and competetitive fitness of the bacterial wilt pathogen Ralston solanacearum. J Bacteriol 188:3697–3708PubMedCrossRefGoogle Scholar
  97. Yarwood CE (1952) Guttation due to leaf pressure favours fungus infections. Phytopathology 42:520Google Scholar
  98. 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 107:1333–1341PubMedCrossRefGoogle Scholar
  99. Zholkevich VN (1992) Root pressure. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Dekker, New York, pp 589–603Google Scholar
  100. Zolobowska L, Van Gijsegem F (2006) Induction of lateral root structure formation on petunia roots: a novel effect of GM11000 Ralston solanacearum infection impaired in Hrp mutants. Mol Plant Microbe Interact 19:597–606PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Plant Sciences, College of Agriculture and Environmental SciencesHaramaya UniversityHaramayaEthiopia

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