Skip to main content
Physiology and Molecular Biology of Plants logoLink to Physiology and Molecular Biology of Plants
. 2008 Jun 15;14(1-2):23–38. doi: 10.1007/s12298-008-0003-5

Hormonal regulation in green plant lineage families

M M Johri 1,
PMCID: PMC3550668  PMID: 23572871

Abstract

The patterns of phytohormones distribution, their native function and possible origin of hormonal regulation across the green plant lineages (chlorophytes, charophytes, bryophytes and tracheophytes) are discussed. The five classical phytohormones — auxins, cytokinins, gibberellins (GA), abscisic acid (ABA) and ethylene occur ubiquitously in green plants. They are produced as secondary metabolites by microorganisms. Some of the bacterial species use phytohormones to interact with the plant as a part of their colonization strategy. Phytohormone biosynthetic pathways in plants seem to be of microbial origin and furthermore, the origin of high affinity perception mechanism could have preceded the recruitment of a metabolite as a hormone. The bryophytes represent the earliest land plants which respond to the phytohormones with the exception of gibberellins. The regulation by auxin and ABA may have evolved before the separation of green algal lineage. Auxin enhances rhizoid and caulonemal differentiation while cytokinins enhance shoot bud formation in mosses. Ethylene retards cell division but seems to promote cell elongation. The presence of responses specific to cytokinins and ethylene strongly suggest the origin of their regulation in bryophytes. The hormonal role of GAs could have evolved in some of the ferns where antheridiogens (compounds related to GAs) and GAs themselves regulate the formation of antheridia.

During migration of life forms to land, the tolerance to desiccation may have evolved and is now observed in some of the microorganisms, animals and plants. Besides plants, sequences coding for late embryogenesis abundant-like proteins occur in the genomes of other anhydrobiotic species of microorganisms and nematodes. ABA acts as a stress signal and increases rapidly upon desiccation or in response to some of the abiotic stresses in green plants. As the salt stress also increases ABA release in the culture medium of cyanobacterium Trichormus variabilis, the recruitment of ABA in the regulation of stress responses could have been derived from prokaryotes and present at the level of common ancestor of green plants. The overall hormonal action mechanisms in mosses are remarkably similar to that of the higher plants. As plants are thought to be monophyletic in origin, the existence of remarkably similar hormonal mechanisms in the mosses and higher plants, suggests that some of the basic elements of regulation cascade could have also evolved at the level of common ancestor of plants. The networking of various steps in a cascade or the crosstalk between different cascades is variable and reflects the dynamic interaction between a species and its specific environment.

Key words: Green plant families, Bryophytes, Abscisic acid, Auxin, Cytokinin, Ethylene, Antheridiogens, miRNA, Origin of hormonal regulation

Full Text

The Full Text of this article is available as a PDF (365.4 KB).

References

  1. Al-Hasani H., Jaenicke L. Characterization of a sex-inducer glycoprotein of Volvox certeri f. weismannia. Sex. Plant Reprod. 1992;5:8–12. doi: 10.1007/BF00714553. [DOI] [Google Scholar]
  2. Anderson L.W.J. Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamogeton nodosus. Science. 1978;201:1135–1138. doi: 10.1126/science.201.4361.1135. [DOI] [PubMed] [Google Scholar]
  3. Arazi T., Talmor-Neiman M., Stav R., Riese M., Huijser P., Baulcombe D.C. Cloning and characterization of micro-RNAs from moss. Plant J. 2005;43:837–848. doi: 10.1111/j.1365-313X.2005.02499.x. [DOI] [PubMed] [Google Scholar]
  4. Ashton N.W., Cove D.J., Featherstone D.R. The isolation and physiological analysis of mutants of the moss Physcomitrella patens. Planta. 1979;144:437–442. doi: 10.1007/BF00380119. [DOI] [PubMed] [Google Scholar]
  5. Assmann S.M. Cyclic AMP as a second messenger in higher plants. Status and Future Prospects. Plant Physiol. 1995;108:885–889. doi: 10.1104/pp.108.3.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Atzorn R., Geier U., Sandberg G. The physiological role of indole acetic acid in the moss Funaria hygrometrica Hedw. I. Quantification of indole-3-acetic acid in tissue and protoplasts by enzyme immunoassay and gas chromatography-mass spectrometry. J. Plant Physiol. 1989;135:522–525. [Google Scholar]
  7. Atzorn R., Bopp M., Merdes U. The physiological role of indole acetic acid in the moss Funaria hygrometrica Hedw. II. Mutants of Funaria hygrometrica which exhibit enhanced catabolism of indole-3-acetic acid. J Plant Physiol. 1989;135:536–530. [Google Scholar]
  8. Axtell M.J., Bartel D.P. Antiquity of microRNAs and their targets in land plants. Plant Cell. 2005;17:1658–1673. doi: 10.1105/tpc.105.032185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Axtell M.J., Snyder J.A., Bartel D.P. Common functions for diverse small RNAs of land plants. Plant Cell. 2007;19:1750–1769. doi: 10.1105/tpc.107.051706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Baldauf S.L., Roger A.L., Wenk-Siefert I., Doolittle W.F. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science. 2000;290:972–977. doi: 10.1126/science.290.5493.972. [DOI] [PubMed] [Google Scholar]
  11. Basile D.V., Basile M.R. Desuppression of leaf primordia of Plagiochila arctica (Hepaticae) by ethylene antagonists. Science. 1983;220:1051–1053. doi: 10.1126/science.220.4601.1051. [DOI] [PubMed] [Google Scholar]
  12. Bauer L. Isolierung und Testung einer kinetinartigen Substanz aus Kalluszellen von Laubmoossporophyten. Z. PflPhysiol. 1966;54:241–253. [Google Scholar]
  13. Bell P.R. The contribution of the ferns to an understanding of the life cycles of vascular plants. In: Dyer A.F., editor. The Experimental Biology of Ferns. London: Academic Press; 1979. pp. 58–85. [Google Scholar]
  14. Benito B., Rodríguez-Navarro A. Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. Plant J. 2003;36:382–389. doi: 10.1046/j.1365-313X.2003.01883.x. [DOI] [PubMed] [Google Scholar]
  15. Beutelmann P., Bauer L. Purification and identification of a cytokinin from moss callus cells. Planta. 1977;133:215–217. doi: 10.1007/BF00380679. [DOI] [PubMed] [Google Scholar]
  16. Bode H.B., Müller R. Possibility of bacterial recruitment of plant genes associated with the biosynthesis of secondary metabolites. Plant Physiol. 2003;132:1153–1161. doi: 10.1104/pp.102.019760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Bopp M. Plant Hormones in Lower Plants. In: Pharis R.P., Rood S., editors. Plant Growth Substances 1988. Berlin: Springer-Verlag; 1990. pp. 1–10. [Google Scholar]
  18. Bopp M., Atzorn R. The morphogenetic system of the moss protonema. Crypt. Bot. 1992;3:3–10. [Google Scholar]
  19. Bopp M., Atzorn R. Hormonelle Regulation der Moosentwicklung. Naturwissenschaften. 1992;79:337–346. doi: 10.1007/BF01140176. [DOI] [Google Scholar]
  20. Bopp M., Werner O. Abscisic acid and desiccation tolerance in mosses. Bot. Acta. 1993;106:103–106. [Google Scholar]
  21. Briggs W.R., Steeves T.A. Morphogenetic studies on Osmunda cinnamomea L. The mechanism of crozier uncoiling. Phytomorphology. 1959;9:134–137. [Google Scholar]
  22. Briggs W.R., Steeves T.A., Sussex I.M., Wetmore R.H. A comparison of auxin destruction by tissue extracts and intact tissues of the fern Osmunda cinnamomea. Plant Physiol. 1955;30:148–155. doi: 10.1104/pp.30.2.148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Brooks K.E. Reproductive biology of Selaginella I. Determination of megasporangia by 2-chloroethylphosphonic acid, an ethylene-releasing compound. Plant Physiol. 1973;51:718–722. doi: 10.1104/pp.51.4.718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Browne J., Tunnacliffe A., Burnell A. Plant desiccation gene found in a nematode. Nature. 2002;416:38. doi: 10.1038/416038a. [DOI] [PubMed] [Google Scholar]
  25. Bürcky K. The occurrence of abscisic acid in Anemia phyllitidis L. Sw. (Schizaeaceae) during ripening of spores. Z. PflPhysiol. 1977;85:181–183. [Google Scholar]
  26. Cheng C.-Y., Schraudolf H. Nachweis von Abscisinsure in Sporen and jungen Prothallien von Anemia phyllitidis L. Sw. Z. PflPhysiol. 1974;71:366–369. [Google Scholar]
  27. Cheng S.-H., Willmann M.R., Chen H.-C., Sheen J. Calcium signalling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 2002;129:469–485. doi: 10.1104/pp.005645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Chernys J., Kende H. Ethylene biosynthesis in Regnellidium diphyllum and Marsilea quadrifolia. Planta. 1996;200:113–118. doi: 10.1007/BF00196657. [DOI] [Google Scholar]
  29. Chia S. E., Raghavan V. Abscisic acid effects on spore germination and protonemal growth in the fern Mohria caffrorum. New Phytol. 1982;92:31–38. doi: 10.1111/j.1469-8137.1982.tb03360.x. [DOI] [Google Scholar]
  30. Conrad P. A., Hepler P. K. The effect of 1,4-dihydropyridines on the initiation and development of gametophore buds in the moss Funaria. Plant Physiol. 1988;86:984–687. doi: 10.1104/pp.86.3.684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Cooke T. J., Poli D. B., Sztein A. E., Cohen J. D. Evolutionary patterns in auxin action. Plant Mol. Biol. 2002;49:319–338. doi: 10.1023/A:1015242627321. [DOI] [PubMed] [Google Scholar]
  32. Cookson C., Osborne D. J. The effect of ethylene and auxin on cell wall extensibility of the semi-aquatic fern Regnellidium diphyllum. Planta. 1979;146:303–307. doi: 10.1007/BF00387802. [DOI] [PubMed] [Google Scholar]
  33. Corey E. J., Meyers A. G. Total synthesis of (I)-antheridium-inducing factor (AAN,2) of the fern Anemia phyllitidis. Clarification of stereochemistry. J. Amer. Chem. Soc. 1985;107:5574–5576. doi: 10.1021/ja00305a067. [DOI] [Google Scholar]
  34. Cove D. J., Ashton N. W. The hormonal regulation of gametophytic development in bryophytes. In: Dyer A.F., Duckett J. G., editors. The Experimental Biology of Bryophytes. London: Academic Press; 1984. pp. 177–201. [Google Scholar]
  35. Döpp W. Eine die Antheridienbildung bei Farnen fordernde Substanz in den Prothallien von Pteridium aquilinum. Ber. Deut. Bot. Des. 1950;63:139–147. [Google Scholar]
  36. D’souza J.S., Johri M.M. Ca2+dPKs from the protonema of the moss Funaria hygrometrica. Effect of indole-acetic acid and cultural parameters on the activity of a 44 kDa Ca2+dPK. Plant Science. 1999;145:23–32. doi: 10.1016/S0168-9452(99)00064-3. [DOI] [Google Scholar]
  37. D’souza J.S., Johri M. M. ABA and NaCl activate myelin basic protein kinase in the chloronema cells of the moss Funaria hygrometrica. Plant Physiol. Biochem. 2002;40:17–24. doi: 10.1016/S0981-9428(01)01344-4. [DOI] [Google Scholar]
  38. D’souza J. S., Johri M. M. Purification and characterization of a Ca2+-dependent/ calmodulin-stimulated protein kinase from moss chloronema cells. J. of Biosciences. 2003;28:223–233. doi: 10.1007/BF02706222. [DOI] [PubMed] [Google Scholar]
  39. Elmore H. W., Whittier D. F. The role of ethylene in the induction of apogamous buds in Pteridium gametophytes. Planta. 1973;111:85–90. doi: 10.1007/BF00386738. [DOI] [PubMed] [Google Scholar]
  40. Elmore H. W., Whittier D. F. Ethylene production and ethylene-induced apogamous bud formation in nine gametophytic strains of Pteridium aquilinum. Ann. Bot. 1975;39:965–971. [Google Scholar]
  41. Fattash I., Voss B., Reski R., Hess W. R., Frank W. Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biology. 2007;7:13. doi: 10.1186/1471-2229-7-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Floyd S.K., Bowman J.L. Gene regulation: ancient microRNA target sequences in plants. Nature. 2004;428:485–486. doi: 10.1038/428485a. [DOI] [PubMed] [Google Scholar]
  43. Gangwani L., Tamot B. K., Khurana J. P., Maheshwari S. C. Identification of 3′-5′-cyclic AMP in axenic cultures of Lemna paucicostata by higher-performance liquid chromato-graphy. Biochem. Biophys. Res. Commun. 1991;178:1113–1119. doi: 10.1016/0006-291X(91)91007-Y. [DOI] [PubMed] [Google Scholar]
  44. Garner L. B., Paolillo D. J. On the function of the stomata in Funaria. Bryologist. 1973;76:423–427. doi: 10.2307/3241726. [DOI] [Google Scholar]
  45. Gillesa G. J., Hinesa K. M., Manfrea A. J., Marcotte W. R., Jr. A predicted N-terminal helical domain of a Group 1 LEA protein is required for protection of enzyme activity from drying. Plant Physiol and Biochem. 2007;45:389–399. doi: 10.1016/j.plaphy.2007.03.027. [DOI] [PubMed] [Google Scholar]
  46. Gorton B. S., Eakin R. E. Development of the gametophyte in the moss Tortella caespitosa. Bot. Gaz. 1957;119:31–38. doi: 10.1086/335957. [DOI] [PubMed] [Google Scholar]
  47. Graham L. G. Green algae to land plants: an evolutionary transition. J. Plant Res. 1996;109:7737–7742. doi: 10.1007/BF02344471. [DOI] [Google Scholar]
  48. Handa A. K., Johri M.M. Cell differentiation by 3′,5′-cyclic AMP in a lower plant. Nature. 1976;259:480–482. doi: 10.1038/259480a0. [DOI] [Google Scholar]
  49. Handa A.K., Johri M.M. Cyclic adenosine 3′,5′-monophosphate in moss protonema. A comparison of its levels by protein kinase and Gilman assays. Plant Physiol. 1977;59:490–496. doi: 10.1104/pp.59.3.490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Handa A.K., Johri M.M. Involvement of cyclic adenosine 3′:5′-monophosphate in chloronema differentiation in protonema cultures of Funaria hygrometrica. Planta. 1979;144:317–324. doi: 10.1007/BF00391574. [DOI] [PubMed] [Google Scholar]
  51. Harmon A.C., Yoo B.-C., Harper J. CDPKs — a kinase for every Ca2+ signal. Trends Plant Sci. 2000;5:154–159. doi: 10.1016/S1360-1385(00)01577-6. [DOI] [PubMed] [Google Scholar]
  52. Hartung, W., Hellwege, E.,M. and Volk, O.,H. (1994). The function of abscisic acid in bryophytes. J. Hattori Bot. Lab., No.76:59–65.
  53. Hartung W., Weiler E.W., Volk O.H. Immunochemical evidence that abscisic acid produced by several species of Anothocerotae and Marchantiales. Bryologist. 1987;90:393–400. doi: 10.2307/3243104. [DOI] [Google Scholar]
  54. Hashimoto K., Sato N. Characterization of the mitochondrial nad7 gene in Physcomitrella patens: similarity with angiosperm nad7 genes. Plant Science. 2001;160:807–815. doi: 10.1016/S0168-9452(00)00444-1. [DOI] [PubMed] [Google Scholar]
  55. Hasunuma K., Funadera K., Furukawa K., Miyamoto-Shinohara Y. Rhythmic oscillation of cyclic 3′,5′-AMP and-GMP concentration and stimulation of flowering by 3′,5′-GMP in Lemna paucicostata 381. Photochem. Photobiol. 1988;48:89–92. doi: 10.1111/j.1751-1097.1988.tb02791.x. [DOI] [Google Scholar]
  56. Hellwege E. M., Volk O. H., Hartung W. A physiological role of abscisic acid in the liverwort Riccia fluitans L. J. Plant Physiol. 1992;140:553–556. [Google Scholar]
  57. Hellwege E. M., Dietz K.-J., Hartung W. Abscisic acid causes changes in gene expression involved in the induction of landform of the liverwort Riccia fluitans L. Planta. 1996;198:423–432. doi: 10.1007/BF00620059. [DOI] [PubMed] [Google Scholar]
  58. Hellwege E. M., Dietz K.-J., Volk O. H., Hartung W. Abscisic acid and the induction of desiccation tolerance in the extremely xerophilic liverwort Exomotheca holstii. Planta. 1994;194:525–531. doi: 10.1007/BF00714466. [DOI] [Google Scholar]
  59. Hickok L.G. Abscisic acid blocks antheridiogen-induced antheridium formation in gametophytes of the fern Ceratopteris richardii. Can. J. Bot. 1983;61:888–892. [Google Scholar]
  60. Hiron, R.W.P. (1974). Effects of physiological stress on natural growth inhibitor level in plants. Ph.D. Thesis, University of London.
  61. Hwang I., Sheen J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature. 2001;413:383–389. doi: 10.1038/35096500. [DOI] [PubMed] [Google Scholar]
  62. Johri M.M. Regulation of cell differentiation and morphogenesis in lower plants. In: Thorpe T.A., editor. Frontiers of Plant Tissue Culture 1978. Calgary, Canada: Univ. of Calgary Offset Printing Services; 1978. pp. 27–36. [Google Scholar]
  63. Johri M.M. Hormonal regulation of development and differentiation in lower plants. In: Sinha S.K., Sane P.V., Bhargava S.C., Agrawal P.K., editors. Proceedings International Congress of Plant Physiology. New Delhi, India: InPrint Exclusives; 1990. pp. 760–775. [Google Scholar]
  64. Johri M. M. Possible origin of hormonal regulation in green plants. Proc Indian Natl. Sci. Acad. 2004;B70(3):335–465. [Google Scholar]
  65. Johri M.M., Desai S. Auxin regulation of caulonema formation in moss protonema. Nature New Biology. 1973;245:223–224. doi: 10.1038/newbio245223a0. [DOI] [PubMed] [Google Scholar]
  66. Johri M.M., D’souza J.S. Auxin Regulation of Cell Differentiation in Moss Protonema. In: Pharis R.P., Rood S., editors. Plant Growth Substances 1988. Berlin: Springer-Verlag; 1990. pp. 407–418. [Google Scholar]
  67. Kamisugi Y., Cuming A.C. The evolution of the abscisic acid-response in land plants: comparative analysis of group1 LEA gene expression in moss and cereal. Plant Mol Biol. 2005;59:723–737. doi: 10.1007/s11103-005-0909-z. [DOI] [PubMed] [Google Scholar]
  68. Karol K.G., McCourt R.M., Climino M.T., Delwiche C.F. The closest living relatives of land plants. Science. 2001;294:2351–2353. doi: 10.1126/science.1065156. [DOI] [PubMed] [Google Scholar]
  69. Kendrick P., Crane P.R. The origin and early evolution of plants on land. Nature. 1997;389:33–39. doi: 10.1038/37918. [DOI] [Google Scholar]
  70. Kim J.H., Cho H.-T., Kende H. á-Expansins in the semiaquatic ferns Marsilea quadrifolia and Regnellidium diphyllum: evolutionary aspects and physiological role in rachis elongation. Planta. 2000;212:85–92. doi: 10.1007/s004250000367. [DOI] [PubMed] [Google Scholar]
  71. Knight C.D., Sehgal A., Atwal K., Wallace J. C., Cove D. J., Coates D., Quatrano R.S., Bahadur S., Stockley P.G., Cuming A.C. Molecular responses to abscisic acid and stress are conserved between moss and cereals. Plant Cell. 1995;7:499–506. doi: 10.1105/tpc.7.5.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Knoop B. In: Development in Bryophytes; in Experimental Biology of Bryophytes. Dyer A. F., Duckett J. G., editors. London: Academic Press; 1984. pp. 143–176. [Google Scholar]
  73. Kochert G. Sexual pheromones in algae and fungi. Annu. Rev. Plant Physiol. 1978;29:461–486. doi: 10.1146/annurev.pp.29.060178.002333. [DOI] [Google Scholar]
  74. Law D.M., Basile D.V., Basile M.R. Determination of endogenous indoleacetic acid in Plagiochila arctica (Hepaticae) Plant Physiol. 1985;77:926–929. doi: 10.1104/pp.77.4.926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Leng Q., Mercier R. W., Yao W., Berkowitz G.A. Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol. 1999;121:753–761. doi: 10.1104/pp.121.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Leveau J.H.J., Lindow S.E. Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Applied and Environmental Microbiol. 2005;71:2365–2371. doi: 10.1128/AEM.71.5.2365-2371.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Lin B.L. In: Heterophylly in Aquatic Plants, in Plant Physiology. Taiz L., Zeiger E., editors. Sunderland, MA, USA: Sinauer Associates Inc.; 2002. [Google Scholar]
  78. Liu B.L.L. Abscisic induces land form characteristics in Marsilia quadrifolia L. Amer. J. Bot. 1984;71:638–644. doi: 10.2307/2443360. [DOI] [Google Scholar]
  79. Ludidi N., Gehring C. Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana. J. Biol. Chem. 2003;278:6490–6494. doi: 10.1074/jbc.M210983200. [DOI] [PubMed] [Google Scholar]
  80. Lunde C., Drew D.P., Jacobs A. K., Tester M. Exclusion of Na+ via sodium ATPase (PpENA1) ensures normal growth of Physcomitrella patens under moderate salt stress. Plant Physiol. 2007;144:1786–1796. doi: 10.1104/pp.106.094946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Maravolo N.C. Polarity and localization of auxin movement in the hepatic Marchantia polymorpha. American J. Bot. 1976;63:529–531. [Google Scholar]
  82. Matsunaga T., Ishii T., Matsumoto S., Higuchi M., Darvill A., Albersheim P., O’Neill M.A. Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol. 2004;134:339–351. doi: 10.1104/pp.103.030072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Michalczuk L., Ribnicky D.M., Cooke T.J., Cohen J.D. Regulation of indole-3-acetic acid biosynthesis pathways in carrot cell cultures. Plant Physiol. 1992;100:1346–1353. doi: 10.1104/pp.100.3.1346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Minorsky P.V. Guanosine-3′,5′-cyclic monophosphate (cGMP) in plants. Plant Physiol. 2003;131:1578–1579. doi: 10.1104/pp.900069. [DOI] [Google Scholar]
  85. Minorsky P.V. Heterophylly in aquatic plants. Plant Physiol. 2003;133:1671–1672. doi: 10.1104/pp.900096. [DOI] [Google Scholar]
  86. Mishler B. D., Lewis L.A., Buchheim M. A., Renzaglia K. S., Garbary D. J., Delwiche C. F., Zechman F. W., Kantz T. S., Chapman R. L. Phylogenetic relationships of the “green algae” and the “bryophytes”. Ann. Mo. Bot. Gard. 1994;81:451–483. doi: 10.2307/2399900. [DOI] [Google Scholar]
  87. Mitra D., Johri M.M. Enhanced expression of a calcium-dependent protein kinase from the moss Funaria hygrometrica under nutritional starvation. J. Biosci. 2000;25:331–338. doi: 10.1007/BF02703786. [DOI] [PubMed] [Google Scholar]
  88. Mohan Ram H.Y., Rao S. In-vitro induction of aerial leaves and of precocious flowering in submerged shoots of limnophila indica by abscisic acid. Planta. 1982;155:521–523. doi: 10.1007/BF01607577. [DOI] [PubMed] [Google Scholar]
  89. Molnár, A., Schwach, F., Studholme, D.J., Thuenemann, E.C. and Baulcombi, D.C. (2007). miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature http://dx.doi.org/10.1038/nature05903. [DOI] [PubMed]
  90. Mount S.M., Cheng C. Evidence for plastid origin of plant ethylene receptor genes. Plant Physiol. 2002;130:10–14. doi: 10.1104/pp.005397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Musgrave A., Walters J. Ethylene and buoyancy control of rachis elongation of the semi-aquatic fern Regnellidium diphyllum. Planta. 1974;121:51–56. doi: 10.1007/BF00384005. [DOI] [PubMed] [Google Scholar]
  92. Nakanishi K., Endo N., Näf U. Structure of the antheridium-inducing factor of the fern Anemia phyllitidis. J. Am. Chem. Soc. 1971;93:5579–5581. doi: 10.1021/ja00750a047. [DOI] [Google Scholar]
  93. Nishiyama T., Fujita T., Shin I. T., Seki M., Nishide H., Uchiyama I., Kamiya A., Carninci P., Hayashizaki Y., Shinozaki K., et al. Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implications for land plant evolution. Proc. Natl. Acad. Sci., USA. 2003;100:8007–8012. doi: 10.1073/pnas.0932694100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Nobles D. R., Romanovicz D. K., Brown R. M. Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? Plant Physiol. 2001;127:529–542. doi: 10.1104/pp.127.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Normanly J., Cohen J. D., Fink G. D. Arabidopsis thaliana auxotrophs reveal a tryptophan-independent biosynthetic pathway for indole-3-acetic acid. Proc. Natl. Acad. Sci., USA. 1993;90:10355–10359. doi: 10.1073/pnas.90.21.10355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Ordog V., Stirk W. A., van Staden J., Novak O., Strnad M. Endogenous cytokinins in three genera of microalgae from the chlorophyta. J. Phycol. 2004;40:88–95. [Google Scholar]
  97. Osborne D.J., Walters J., Milborrow B.V., Norville A., Stange L.M.C. Evidence for a non-ACC ethylene bio-synthesis pathway in lower plants. Phytochemistry. 1996;42:51–60. doi: 10.1016/0031-9422(96)00032-5. [DOI] [Google Scholar]
  98. Pasternak T. P., Prinsen E., Ayaydin F., Miskolczi P., Potters G., Asard H., Van Onckelen H. A., Dudits D., Feher A. The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplasts-derived cells of Alfalfa. Plant Physiol. 2002;129:1807–1819. doi: 10.1104/pp.000810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Peterson R. L. Callus induction in Ophioglossum petiolatum Hook. Can. J. Bot. 1967;45:2225–2227. [Google Scholar]
  100. Pirozynski K.A., Malloch D.W. The origin of land plants: a matter of mycotrophism. BioSystems. 1975;6:153–164. doi: 10.1016/0303-2647(75)90023-4. [DOI] [PubMed] [Google Scholar]
  101. Poli D.B., Jacobs M., Cooke T.J. Auxin regulation of axial growth in bryophyte sporophytes: its potential significance for the evolution of early land plants. American J. Bot. 2003;90:1405–1415. doi: 10.3732/ajb.90.10.1405. [DOI] [PubMed] [Google Scholar]
  102. Proctor M. Patterns of desiccation tolerance and recovery in bryophytes. Plant Growth Regulation. 2001;35:147–156. doi: 10.1023/A:1014429720821. [DOI] [Google Scholar]
  103. Redecker D., Kodner R., Graham L.E. Glomalean fungi from the Ordovician. Science. 2000;289:1920–1921. doi: 10.1126/science.289.5486.1920. [DOI] [PubMed] [Google Scholar]
  104. Rensing S. A., Rombauts S., Van de Peer Y., Reski R. Moss transcriptome and beyond. Trends in Pl. Sci. 2002;7:535–538. doi: 10.1016/S1360-1385(02)02363-4. [DOI] [PubMed] [Google Scholar]
  105. Renzaglia K. S., Duff R. J., Nickrent D. L., Garbary D. J. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Phil. Trans. R. Soc. Lond. 2000;B355:769–793. doi: 10.1098/rstb.2000.0615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Reski R., Reynolds S., Wehe M., Kleber-Janke T., Kruse S. Moss (Physcomitrella patens) expressed sequence tags include several sequences which are novel for plants. Bot. Acta. 1998;111:1–7. [Google Scholar]
  107. Reynolds T. L. Effects of auxin and abscisic acid on adventitious gametophyte formation by Anemia phyllitidis. Z. PflPhysiol. 1981;103:9–14. [Google Scholar]
  108. Reynolds T.L., Bewley J.D. Characterization of protein synthetic changes in a desiccation-tolerant fern, Polypodium virginianum. Comparison of the effects of drying, rehydration and abscisic acid. J. Exp. Bot. 1993;44:921–928. doi: 10.1093/jxb/44.5.921. [DOI] [Google Scholar]
  109. Rohwer R., Bopp M. Ethylene synthesis in moss protonema. J. Plant Physiol. 1985;117:331–338. doi: 10.1016/S0176-1617(85)80069-9. [DOI] [PubMed] [Google Scholar]
  110. Rose S., Bopp M. Uptake and polar transport of indoleacetic acid in moss rhizoids. Physiol Plant. 1983;58:57–61. doi: 10.1111/j.1399-3054.1983.tb04143.x. [DOI] [Google Scholar]
  111. Russell A. J., Knight M. R., Cove D. J., Knight C. D., Trewavas A. J., Wang T. L. The moss, Physcomitrella patens, transformed with apoaequorin cDNA responds to cold, shock, mechanical perturbation and pH transient increases in cytoplasmic calcium. Transgenic Res. 1996;5:167–170. doi: 10.1007/BF01969705. [DOI] [PubMed] [Google Scholar]
  112. Saavedra L., Svensson J., Carbaffo V., Izmendi D., Wefin B., Vidal S. A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J. 2006;45:237–249. doi: 10.1111/j.1365-313X.2005.02603.x. [DOI] [PubMed] [Google Scholar]
  113. Sakakibara K., Nishiyama T., Sumikawa N., Kofuji R., Murata T., Hasebe M. Involvement of auxin and homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development. 2003;130:4835–4846. doi: 10.1242/dev.00644. [DOI] [PubMed] [Google Scholar]
  114. Schaefer D.G., Zrÿd J.-P. Efficient gene targeting in the moss Physcomitrella patens. Plant J. 1997;11:1195–1206. doi: 10.1046/j.1365-313X.1997.11061195.x. [DOI] [PubMed] [Google Scholar]
  115. Schneider E. A., Wightman F. Auxins of nonflowering plants. I. Occurrence of IAA and phenylacetic acid in vegetative and fertile fronds of ostrich fern (Matteucia struthiopteris) Physiol. Plant. 1986;68:396–402. doi: 10.1111/j.1399-3054.1986.tb03372.x. [DOI] [Google Scholar]
  116. Schipper O., Schaefer D., Reski R., Fleming A. Expansins in the bryophyte Physcomitrella patens. Plant Mol. Biol. 2002;50:789–802. doi: 10.1023/A:1019907207433. [DOI] [PubMed] [Google Scholar]
  117. Schraudolf H. Action and phylogeny of antheridiogens. Proc. Royal Soc. Edinb. 1985;86B:75–80. [Google Scholar]
  118. Schraudolf H. Phytohormones and Filicinae: chemical signals triggering morphogenesis in Schizaeaceae. In: Bopp M., editor. Plant Growth Substances 1985. Berlin: Springer-Verlag; 1986. pp. 270–274. [Google Scholar]
  119. Schulz P.A., Hofmann A. H., Russo V. E. A., Hartmann E., Laloue M., Schwartzenberg V.K. Cytokinin overproducing ove mutants of Physcomitrella patens show increased riboside to base conversion. Plant Physiol. 2001;126:1224–1231. doi: 10.1104/pp.126.3.1224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Schumaker K. S., Gizinski M. J. G proteins regulate dihydropyridine binding sites in moss plasma membranes. J. Biol. Chem. 1996;271:21292–21296. doi: 10.1074/jbc.271.35.21292. [DOI] [PubMed] [Google Scholar]
  121. Sharma S., Johri M.M. Partial purification and characterization of cyclic AMP phosphodiesterase from Funaria hygrometrica. Arch Biochem. Biophys. 1982;21:87–97. doi: 10.1016/0003-9861(82)90482-9. [DOI] [PubMed] [Google Scholar]
  122. Sievers A., Schröter K. Versuch einer Kausalanalyse der geotropischen Reaktionskette im Chara-Rhizoid. Planta. 1971;96:339–353. doi: 10.1007/BF00386948. [DOI] [PubMed] [Google Scholar]
  123. Spaepen S., Vanderleyden J., Remans R. Indole-3-acetic acid in microbial and microorganism-plant signalling. FEMS Microbiol Rev. 2007;31:1–24. doi: 10.1111/j.1574-6976.2007.00072.x. [DOI] [PubMed] [Google Scholar]
  124. Stirk W.A., Novák O., Strnad M., van Staden J. Cytokinins in macroalgae. Plant Growth Regulation. 2003;41:13–24. doi: 10.1023/A:1027376507197. [DOI] [Google Scholar]
  125. Sugai M., Nakamura K., Yamane H., Sato Y., Takahashi N. Effects of gibberellins and their methyl esters on dark germination and antheridium formation in Lygodium and Anemia phyllitidis. Plant Cell Physiol. 1987;28:199–202. [Google Scholar]
  126. Sztein A. E., Cohen J. D., Cooke T. J. Evolutionary patterns in the auxin metabolism in green plants. Int. J. Plant Sci. 2000;161:849–859. doi: 10.1086/317566. [DOI] [Google Scholar]
  127. Sztein A. E., Cohen J. D., de la Feuente I. G., Cooke T. J. Auxin metabolism in mosses and liverworts. American J. Bot. 1999;86:1544–1555. doi: 10.2307/2656792. [DOI] [PubMed] [Google Scholar]
  128. Sztein A. E., Iliæ N., Cohen J. D., Cooke T. J. Indole-3-acetic acid biosynthesis in isolated axes from germinating bean seeds: The effect of wounding on the biosynthetic pathway. Plant Growth Regulation. 2002;36:201–207. doi: 10.1023/A:1016586401506. [DOI] [Google Scholar]
  129. Takeno K., Furuya M. Sporophyte formation in experimentally induced unisexual female and bisexual gametophytes of Lygodium japonicum. Bot. Mag. 1987;100:37–41. doi: 10.1007/BF02488418. [DOI] [Google Scholar]
  130. Thomas R. J., Harrison M. A., Taylor J., Kaufman P. B. Endogenous auxin and ethylene in Pellia (Bryophyta) Plant Physiol. 1983;73:395–397. doi: 10.1104/pp.73.2.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Thummler F., Dufner M., Kreisl P., Dittrich P. Molecular cloning of a novel phytochrome gene of the moss Ceratodon purpureus which encodes a putative light-regulated protein kinase. Plant Mol. Biol. 1992;20:1003–1017. doi: 10.1007/BF00028888. [DOI] [PubMed] [Google Scholar]
  132. Tietz, A., Köhler, R., Ruttkowski, U. and Kasprik, W. (1987). Further investigations on the occurrence and the effects of abscisic acid in algae. Proc. XIV Intl. Bot. Congr., Berlin. Abst. 2-113b-7.
  133. Urao T., Yamaguchi-Shinozaki K., Shinozaki K. Two-component systems in plant signal transduction. Trends Plant Sci. 2000;5:67–75. doi: 10.1016/S1360-1385(99)01542-3. [DOI] [PubMed] [Google Scholar]
  134. Valdon L. R. G., Mummery R. S. Quantitative relationship between various growth substances and bud production in Funaria hygrometrica. A bioassay for abscisic acid. Physiol Plant. 1971;24:232–234. doi: 10.1111/j.1399-3054.1971.tb03484.x. [DOI] [Google Scholar]
  135. von Schwartzenberg K., Núñez M. F., Blaschke H., Dobrev P.I., Novák O., Motyka V., Strnad M. Cytokinins in the bryophyte Physcomitrella patens: analyses of activity, distribution, and cytokinin oxidase/dehydrogenase overexpression reveal the role of extracellular cytokinin. Pl. Physiol. 2007;145:786–800. doi: 10.1104/pp.107.103176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Waaland S. D. Hormonal coordination of the processes leading to cell fusion in algae: a glycoprotein hormone from red algae. In: Bopp M., editor. Plant Growth Substances 1985. Berlin: Springer-Verlag; 1986. pp. 257–262. [Google Scholar]
  137. Walters J., Osborne D. J. Ethylene and auxin-induced growth in relation to auxin transport and metabolism and ethylene production in the semi-aquatic plant. Regnellidium diphyllum. Planta. 1979;146:309–317. doi: 10.1007/BF00387803. [DOI] [PubMed] [Google Scholar]
  138. Waters E. R., Vierling E. The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Mol. Biol. Evol. 1999;16:127–139. doi: 10.1093/oxfordjournals.molbev.a026033. [DOI] [PubMed] [Google Scholar]
  139. Webster T. R. An investigation of angle meristem development in excised stem segments of Selaginella martensii. Can. J. Bot. 1969;47:255–263. [Google Scholar]
  140. Werner O., Bopp M. The influence of ABA and IAA on in vitro phosphorylation of proteins of Funaria hygrometrica. J. Plant Physiol. 1993;141:93–97. [Google Scholar]
  141. Werner O., Ros-Espin R. M., Bopp M., Atzorn R. Abscisic acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta. 1991;186:99–103. doi: 10.1007/BF00201503. [DOI] [PubMed] [Google Scholar]
  142. Wochok Z. S., Sussex I. M. Morphogenesis in Selaginella. II. Auxin transport in the root (rhizophore) Plant Physiol. 1974;53:738–741. doi: 10.1104/pp.53.5.738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Wochok Z. S., Sussex I. M. Morphogenesis in Selaginella. III. Meristem determination and cell differentiation. Dev. Biol. 1975;47:376–383. doi: 10.1016/0012-1606(75)90291-2. [DOI] [PubMed] [Google Scholar]
  144. Wood A. J., Duff R. J., Oliver M. J. Expressed sequence tags (ESTs) from desiccated Tortula ruralis identify a large number of novel plant genes. Plant Cell Physiol. 1999;40:361–368. doi: 10.1093/oxfordjournals.pcp.a029551. [DOI] [PubMed] [Google Scholar]
  145. Wright A. D., Sampson M. B., Neuffer M. G., Michalczuk L., Slovin J. S., Cohen J.D. Indole-3-Acetic Acid biosynthesis in the mutant maize orange pericarp, a tryptophan auxotroph. Science. 1991;254:998–1000. doi: 10.1126/science.254.5034.998. [DOI] [PubMed] [Google Scholar]
  146. Yamane H., Takahashi N., Takeno K., Furuya M. Identification of gibberellin A9 methyl ester as a natural substance regulating formation of reproductive organs in Lygodium japonicum. Planta. 1979;147:251–256. doi: 10.1007/BF00388747. [DOI] [PubMed] [Google Scholar]
  147. Yamane H., Watanabe M., Satoh Y., Takahashi N., Iwatsuki K. Identification of cytokinins in two species of pteridophyte sporophytes. Plant Cell Physiol. 1983;24:1027–1032. [Google Scholar]
  148. Young J.P., Horton R.F. Heterophylly in Rananculus flabellaris: the effect of abscisic acid. Ann. Bot. 1985;55:899–902. [Google Scholar]
  149. Zahradnicková H., Marðálek B., Poliðenská M. High-performance thin-layer chromatographic and high-performance liquid chromatographic determination of abscisic acid produced by cyanobacteria. J. of Chromatograph, A. 1991;555:239–245. doi: 10.1016/S0021-9673(01)87184-3. [DOI] [Google Scholar]
  150. Zhang B., Pan X., Cannon C. H., Cobb G. P., Anderson T. A. Conservation and divergence of plant microRNA genes. Plant J. 2006;46:243–259. doi: 10.1111/j.1365-313X.2006.02697.x. [DOI] [PubMed] [Google Scholar]
  151. Zhao T., Li G., Mi S., Li S., Hannon G. J., Wang X. J., Qi Y. A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev. 2007;21:1190–1203. doi: 10.1101/gad.1543507. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Physiology and molecular biology of plants : an international journal of functional plant biology are provided here courtesy of Springer

RESOURCES