Green Algae and the Origins of Multicellularity in the Plant Kingdom

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 11, 2014, Pages

  Umen, James G ^a  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYTA;

ANATOMY AND HISTOLOGY; CELL DIFFERENTIATION; CYTOLOGY; EVOLUTION; GENETICS; GREEN ALGA; GROWTH, DEVELOPMENT AND AGING; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT CELL; REPRODUCTION;

BIOLOGICAL EVOLUTION; CELL DIFFERENTIATION; CHLOROPHYTA; PHYLOGENY; PLANT CELLS; PLANTS; REPRODUCTION;

EID: 84908430742     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016170     Document Type: Article

References (241)

1. Adair WS, Steinmetz SA, Mattson DM, Goodenough U., Heuser JE. 1987. Nucleated assembly of Chlamydomonas and Volvox cell walls. J Cell Biol 105: 2373-2382.
2. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, et al. 2012. The revised classification of Eukaryotes. J Eukaryot Microbiol 59: 429-514.
3. Alegado RA, King N. 2014. Bacterial influences on animal origins. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016162.
4. Ariizumi T, Toriyama K. 2011. Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62: 437-460.
5. Baluška F, Volkmann D, Barlow PW. 2004. Eukaryotic cells and their cell bodies: Cell theory revised. Ann Bot 94: 9-32.
6. Beardall J, Allen D, Bragg J, Finkel Z, Flynn K, Quigg A, Rees T, Richardson A, Raven J. 2009. Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytologist 181: 295-309.
7. Becker B, Marin B. 2009. Streptophyte algae and the origin of embryophytes. Ann Bot 103: 999-1004.
8. Beilby MJ, Casanova MT. 2014. The physiology of Characean cells. Springer, Berlin.
9. Bell G. 1985. The origin and early evolution of germ cells as illustrated by the Volvocales. In The origin and evolution of sex (ed. HalvorsonHO,Monroy A), pp. 221-256. Alan R. Liss, New York.
10. Berney C, Pawlowski J. 2006. A molecular time-scale for eukaryote evolution recalibratedwith the continuous microfossil record. Proc Biol Sci 273: 1867-1872.
11. Besson S, Dumais J. 2011. Universal rule for the symmetric division of plant cells. ProcNatlAcad Sci 108: 6294-6299.
12. Bhattacharya D, Weber K, An SS, Berning-Koch W. 1998. Actin phylogeny identifies Mesostigma viride as a flagellate ancestor of the land plants. J Mol Evol 47: 544-550.
13. Boot KJM, Libbenga KR, Hille SC, Offringa R, van Duijn B. 2012. Polar auxin transport: An early invention. J Exp Bot 63: 4213-4218.
14. Boraas ME, Seale DB, Boxhorn JE. 1998. Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity. Evol Ecol 12: 153-164.
15. Bowman JL. 2013.Walkabout on the long branches of plant evolution. Curr Opin Plant Biol 16: 70-77.
16. Bowman JL, Floyd SK, Sakakibara K. 2007. Green genescomparative genomics of the green branch of life. Cell 129: 229-234.
17. Boyce CK, Zwieniecki MA, Cody GD, Jacobsen C, Wirick S, Knoll AH, Holbrook NM. 2004. Evolution of xylem lignification and hydrogel transport regulation. Proc Natl Acad Sci 101: 17555-17558.
18. Bradley PM. 1991. Plant hormones do have a role in controlling growth and development of algae. J Phycol 27: 317-321.
19. Braun M, Limbach C. 2006. Rhizoids and protonemata of characean algae: Model cells for research on polarized growth and plant gravity sensing. Protoplasma 229: 133-142.
20. Brooks J, Shaw G. 1978. Sporopollenin: A review of its chemistry, palaeochemistry and geochemistry. Grana 17: 91-97.
21. Buss LW. 1987. The evolution of individuality. PrincetonUniversity Press, Princeton.
22. Cheng Q, Fowler R, Tam L-W, Edwards L, Miller SM. 2003. The role of GlsA in the evolution of asymmetric cell division in the green alga Volvox carteri. Dev Genes Evol 213: 328-335.
23. Cheng Q, Pappas V, Hallmann A, Miller SM. 2005. Hsp70A and GlsA interact as partner chaperones to regulate asymmetric division in Volvox. Dev Biol 286: 537-548.
24. Cocquyt E, Verbruggen H, Leliaert F, De Clerck O. 2010. Evolution and cytological diversification of the green seaweeds (Ulvophyceae). Mol Biol Evol 27: 2052-2061.
25. Coleman AW. 2012. A comparative analysis of the Volvocaceae (Chlorophyta). J Phycol 48: 491-513.
26. Cook ME. 2004. Cytokinesis in Coleochaete orbicularis (Charophyceae): An ancestral mechanism inherited by plants. Am J Bot 91: 313-320.
27. Cook ME, Graham LE, Lavin CA. 1998. Cytokinesis and nodal anatomy in the charophycean green alga Chara zeylanica. Protoplasma 203: 65-74.
28. Cooke TJ, Poli D, Sztein AE, Cohen JD. 2002. Evolutionary patterns in auxin action. Plant Mol Biol 49: 319-338.
29. Cosgrove DJ. 2000. Loosening of plant cell walls by expansins. Nature 407: 321-326.
30. Cutler SR, Rodriguez PL. 2010. Abscisic acid: Emergence of a core signaling network. Annu Rev Plant Biol 61: 651-679.
31. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K, King N. 2011. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357: 73-82.
32. De Clerck O, Bogaert KA, Leliaert F. 2012. Diversity and evolution of algae. In Advances in botanical research, Vol. 64, pp. 55-86. Elsevier, Amsterdam.
33. Degnan BM, Vervoort M, Larroux C, Richards GS. 2009. Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19: 591-599.
34. De Hoff PL, Ferris P, Olson BJSC, Miyagi A, Geng S, Umen JG. 2013. Species and population level molecular profiling reveals cryptic recombination and emergent asymmetry in the dimorphic mating locus of C. reinhardtii. PLoS Genet 9: e1003724.
35. Delwiche CF, Graham LE, Thomson N. 1989. Lignin-like compounds and sporopollenin coleochaete, an algal model for land plant ancestry. Science 245: 399-401.
36. Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynié S, Cooke R, et al. 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci 103: 11647-11652.
37. de Saint Germain A, Bonhomme S, Boyer F-D, Rameau C. 2013. Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol 16: 583-589.
38. De Smet I, Beeckman T. 2011. Asymmetric cell division in land plants and algae: The driving force for differentiation. Nat Rev Mol Cell Biol 12: 177-188.
39. De Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, et al. 2011. Unraveling the evolution of auxin signaling. Plant Physiol 155: 209-221.
40. Desnitski A. 1995.A reviewon the evolution of development in Volvox-morphological and physiological aspects. Eur J Protist 31: 241-247.
41. Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WG. 2012. The cell walls of green algae: A journey through evolution and diversity. Front Plant Sci 3.
42. Donnan L, John PC. 1983. Cell cycle control by timer and sizer in Chlamydomonas. Nature 304: 630-633.
43. Dring MJ. 1988. Photocontrol of development in algae. Annu Rev Plant Physiol Plant Mol Biol 39: 157-174.
44. Duncan L, Nishii I, Howard A, Kirk D, Miller SM. 2006. Orthologs and paralogs of regA, a master cell-type regulatory gene in Volvox carteri. Curr Genet 50: 61-72.
45. Duncan L, Nishii I, Harryman A, Buckley S, Howard A, Friedman NR, Miller SM. 2007.
46. The VARL gene family and the evolutionary origins of the master cell-type regulatory gene, regA, in Volvox carteri. JMol Evol 65: 1-11.
47. Dupuy L, Mackenzie J, Haseloff J. 2010. Coordination of plant cell division and expansion in a simple morphogenetic system. Proc Natl Acad Sci 107: 2711-2716.
48. Ehler LL, Dutcher SK. 1998. Pharmacological and genetic evidence for a role of rootlet and phycoplast microtubules in the positioning and assembly of cleavage furrows in Chlamydomonas reinhardtii. Cell Motil Cytoskeleton 40: 193-207.
49. Ehler LL, Holmes JA, Dutcher SK. 1995. Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies. Genetics 141: 945-960.
50. Elhiti M, Stasolla C. 2009. Structure and function of homodomain-leucine zipper (HD-Zip) proteins. Plant Signal Behav 4: 86-88.
51. Emiliani G, Fondi M, Fani R, Gribaldo S. 2009. A horizontal gene transfer at the origin of phenylpropanoid metabolism: A key adaptation of plants to land. Biol Direct 4: 7.
52. Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ, et al. 2013. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14: R15.
53. Fang S-C, de los Reyes C, Umen JG. 2006. Cell size checkpoint control by the retinoblastoma tumor suppressor pathway. PLoS Genet 2: e167.
54. Faulkner CR, Blackman LM, Cordwell SJ, Overall RL. 2005. Proteomic identification of putative plasmodesmatal proteins from Chara corallina. Proteomics 5: 2866-2875.
55. Ferris PJ, Goodenough UW. 1997. Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics 146: 859-869.
56. Ferris P, Olson BJSC, De Hoff PL, Douglass S, Casero D, Prochnik S, Geng S, Rai R, Grimwood J, Schmutz J, et al. 2010. Evolution of an expanded sex-determining locus in Volvox. Science 328: 351-354.
57. Finet C, Timme RE, Delwiche CF, Marlétaz F. 2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr Biol 20: 2217-2222.
58. Floyd SK, Bowman JL. 2007. The ancestral developmental tool kit of land plants. Int J Plant Sci 168: 1-35.
59. Floyd GL, Stewart KD, Mattox KR. 1972. Cellular organization, mitosis, and cytokinesis in the Ulotrichalean Alga, Klebsormidium. J Phycol 8: 176-184.
60. Floyd SK, Zalewski CS, Bowman JL. 2006. Evolution of class III homeodomain-leucine zipper genes in streptophytes. Genetics 173: 373-388.
61. Fowke LC, Pickett-Heaps JD. 1969. Cell division in Spirogyra: II. Cytokinesis. J Phycol 5: 273-281.
62. Franceschi VR, Ding B, Lucas WJ. 1994.Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular communication in higher plants. Planta 192: 347-358.
63. Fritsch FE. 1948. The structure and reproduction of the algae. Cambridge University Press, Cambridge.
64. Galway ME, Hardham AR. 1991. Immunofluorescent localization of microtubules throughout the cell cycle in the green alga Mougeotia (Zygnemataceae). Am J Bot 78: 451-461.
65. Graham LE. 1984.Coleochaete and the origin of land plants. Am J Bot 71: 603-608.
66. Graham LE. 1996. Green algae to land plants: An evolutionary transition. J Plant Res 109: 241-251.
67. Graham LE, Wilcox LW. 1983. The occurrence and phylogenetic significance of putative placental transfer cells in the green alga Coleochaete. Am J Bot 70: 113-120.
68. Graham LK, Wilcox LW. 2000. The origin of alternation of generations in land plants: A focus on matrotrophy and hexose transport. Philos Trans R Soc Lond B Biol Sci 355: 757-766; discussion 766-767.
69. Graham LE, Cook ME, Busse JS. 2000. The origin of plants: Body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci 97: 4535-4540.
70. Graham LE, Graham JM, Wilcox LW. 2009. Algae. Benjamin-Cummings, San Francisco.
71. Graham LE, Arancibia-Avila P, Taylor WA, Strother PK, Cook ME. 2012. Aeroterrestrial Coleochaete (Streptophyta, Coleochaetales) models early plant adaptation to land. Am J Bot 99: 130-144.
72. Grauvogel C, Petersen J. 2007. Isoprenoid biosynthesis authenticates the classification of the green alga Mesostigma viride as an ancient streptophyte. Gene 396: 125-133.
73. Green KJ, Viamontes GI, Kirk DL. 1981. Mechanism of formation, ultrastructure, and function of the cytoplasmic bridge system during morphogenesis in Volvox. J Cell Biol 91: 756-769.
74. Greuel BT, Floyd GL. 1985. Development of the flagellar apparatus and flagellar orientation in the colonial green alga Gonium pectorale (Volvocales). J Phycol 21: 358-371.
75. Grosberg R, Strathmann R. 2007. The evolution of multicellularity: A minor major transition? Annu Rev Ecol Evol Syst 38: 621-654.
76. Güde H. 1979. Grazing by protozoa as selection factor for activated sludge bacteria. Microb Ecol 5: 225-237.
77. Gunnison D, Alexander M. 1975. Basis for the resistance of several algae to microbial decomposition. Appl Microbiol 29: 729-738.
78. Gutzat R, Borghi L, Gruissem W. 2012. Emerging roles of RETINOBLASTOMA-RELATED proteins in evolution and plant development. Trends Plant Sci 17: 139-148.
79. Hackenberg D, Sakayama H, Nishiyama T, Pandey S. 2013. Characterization of the heterotrimeric G-protein complex and its regulator from the green alga Chara braunii expands the evolutionary breadth of plant G-protein signaling. Plant Physiol 163: 1510-1517.
80. Haig D. 2010. What do we know about Charophyte (Streptophyta) life cycles? J Phycol 46: 860-867.
81. Hall JD, McCourt RM, Delwiche CF. 2008. Patterns of cell division in the filamentous Desmidiaceae, close green algal relatives of land plants. Am J Bot 95: 643-654.
82. Hallmann A. 2003. Extracellular matrix and sex-inducing pheromone in Volvox. Int Rev Cytol 227: 131-182.
83. Hallmann A. 2006a. Morphogenesis in the family Volvocaceae: Different tactics for turning an embryo right-side out. Protist 157: 445-461.
84. Hallmann A. 2006b. The pherophorins: Common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales. Plant J 45: 292-307.
85. Hamaji T, Ferris PJ, Coleman AW, Waffenschmidt S, Takahashi F, Nishii I, Nozaki H. 2008. Identification of the minus-dominance gene ortholog in the mating-type locus of Gonium pectorale. Genetics 178: 283-294.
86. Hamaji T, Ferris PJ, Nishii I, Nishimura Y, Nozaki H. 2013. Distribution of the sex-determining gene MID and molecular correspondence of mating types within the isogamous genus Gonium (Volvocales, Chlorophyta). PLoS ONE 8: e64385.
87. Hartung W. 2010. The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37: 806.
88. Hauser F, Waadt R, Schroeder JI. 2011. Evolution of abscisic acid synthesis review and signaling mechanisms. Curr Biol 21: R346-R355.
89. Hayama M, Nakada T, Hamaji T, Nozaki H. 2010.Morphology, molecular phylogeny and taxonomy of Gonium maiaprilis sp. nov. (Goniaceae, Chlorophyta) fromJapan. Phycologia 49: 221-234.
90. Hegemann P. 2008. Algal sensory photoreceptors—Annual review of plant biology. Annu Rev Plant Biol 59: 167.
91. Heitzer M, Hallmann A. 2002. An extracellular matrix-localized metalloproteinase with an exceptional QEXXH metal binding site prefers copper for catalytic activity. J Biol Chem 277: 28280-28286.
92. Hepler PK. 1982. Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111: 121-133.
93. Hernández-Hernández V, Niklas KJ, Newman SA, Benítez M. 2012. Dynamical patterning modules in plant development and evolution. Int J Dev Biol 56: 661-674.
94. Herron MD, Michod RE. 2008. Evolution of complexity in the volvocine algae: Transitions in individuality through Darwin’s eye. Evolution 62: 436-451.
95. Herron MD, Hackett JD, Aylward FO, Michod RE. 2009. Triassic origin and early radiation of multicellular volvocine algae. Proc Natl Acad Sci 106: 3254-3258.
96. Höhn S, Hallmann A. 2011. There is more than one way to turn a spherical cellular monolayer inside out: Type B embryo inversion in Volvox globator. BMC Biol 9: 89.
97. Holmes JA, Dutcher SK. 1989. Cellular asymmetry in Chlamydomonas reinhardtii. J Cell Sci 94: 273-285.
98. Hoops HJ. 1984. Somatic cell flagellar apparatuses in two species of Volvox (Chlorophyceae). J Phycol 20: 20-27.
99. Huskey RJ, Griffin BE. 1979. Genetic control of somatic cell differentiation in Volvox analysis of somatic regenerator mutants. Dev Biol 72: 226-235.
100. Imahori K, Iwasa K. 1965. Pure culture and chemical regulation of the growth of charophytes. Phycologia 4: 127-134.
101. Ispolatov I, Ackermann M, Doebeli M. 2012. Division of labour and the evolution of multicellularity. Proc Biol Sci 279: 1768-1776.
102. Jacobs WP. 1970. Development and regeneration of the algal giant coenocyte Caulerpa. Ann NY Acad Sci 175: 732-748.
103. Jin Q, Scherp P, Heimann K, Hasenstein KH. 2008. Auxin and cytoskeletal organization in algae. Cell Biol Int 32: 542-545.
104. John P. 1987. Control points in the Chlamydomonas cell cycle. In Algal development (ed. Wiessner W, Robinson DG, Starr RC), Springer, Berlin.
105. Johnson UG, Porter KR. 1968. Fine structure of cell division in Chlamydomonas reinhardi. Basal bodies and microtubules. J Cell Biol 38: 403-425.
106. Johri MM. 2004. Possible origin of hormonal regulation in green plants. Proc Natl Acad Sci India B 70: 335-365.
107. Katsaros CI, Varvarigos V, Gachon CMM, Brand J, Motomura T, Nagasato C, Küpper FC. 2011. Comparative immunofluorescence and ultrastructural analysis of microtubule organization in Uronema sp., Klebsormidium flaccidum, K. subtilissimum, Stichococcus bacillaris and S. chloranthus (Chlorophyta). Protist 162: 315-331.
108. Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud P-F, Pan A, Quatrano RS. 2010. Role of ABA and ABI3 in desiccation tolerance. Science 327: 546.
109. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783-788.
110. Kirk DL. 1988. The ontogeny and phylogeny of cellular differentiation in Volvox. Trends Genet 4: 32-36.
111. Kirk DL. 1998. Volvox. Cambridge University Press, Cambridge.
112. Kirk DL. 2003. Seeking the ultimate and proximate causes of Volvox multicellularity and cellular differentiation. Integr Comp Biol 43: 247-253.
113. Kirk DL. 2005. A twelve-step program for evolving multicellularity and a division of labor. BioEssays 27: 299-310.
114. Kirk D., Birchem R, King N. 1986. The extracellular matrix of Volvox: A comparative study and proposed system of nomenclature. J Cell Sci 80: 207-231.
115. Kirk D., Kaufman MR, Keeling RM, Stamer KA. 1991. Genetic and cytological control of the asymmetric divisions that pattern the Volvox embryo. Dev Suppl 1: 67-82.
116. Kirk MM, Ransick A, McRae SE, Kirk DL. 1993. The relationship between cell size and cell fate in Volvox carteri. J Cell Biol 123: 191-208.
117. Kirk MM, Stark K, Miller SM, Müller W, Taillon BE, Gruber H, Schmitt R, Kirk DL. 1999. regA, a Volvox gene that plays a central role in germ-soma differentiation, encodes a novel regulatory protein. Development 126: 639-647.
118. Klämbt D, Knauth B, Dittmann I. 1992. Auxin dependent growth of rhizoids of Chara globularis. Physiol Plant 85: 537-540.
119. Knoll AH. 2011. The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci 39: 217-239.
120. Koufopanou V. 1994. The evolution of soma in the Volvocales. Am Nat 143: 907-931.
121. Kwiatkowska M. 2003. Plasmodesmal changes are related to different developmental stages of antheridia of Chara species. Protoplasma 222: 1-11.
122. Kwiatkowska M, Wojtczak A, Poptoriska K. 1998. Effect of GA3 treatment on the number of spermatozoids and endopolyploidy levels of non-generative cells in Antheridia of Chara vulgaris L. Plant Cell Physiol 39: 1388-1390.
123. Langdale JA, Harrison CJ. 2008. Developmental transitions during the evolution of plant form. In Evolving pathways: Key themes in evolutionary developmental biology (ed. Minelli A), pp. 299-316. Cambridge University Press, Cambridge.
124. Lau S, Shao N, Bock R, Jurgens G, De Smet I. 2009. Auxin signaling in algal lineages: Fact or myth? Trends Plant Sci 14: 182-188.
125. Laurin-Lemay S, Brinkmann H, Philippe H. 2012. Origin of land plants revisited in the light of sequence contamination and missing data. Curr Biol 22: R593-R594.
126. Lee J-H, Lin H, Joo S, Goodenough U. 2008. Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133: 829-840.
127. Lee J-H, Waffenschmidt S, Small L, Goodenough U. 2007. Between-species analysis of short-repeat modules in cell wall and sex-related hydroxyproline-rich glycoproteins of Chlamydomonas. Plant Physiol 144: 1813-1826.
128. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O. 2012. Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31: 1-46.
129. Lemieux C, Otis C, Turmel M. 2000. Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403: 649-652.
130. Lemieux C, Otis C, Turmel M. 2007. A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biol 5: 2.
131. Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants. Am J Bot 91: 1535-1556.
132. Ligrone R, Duckett JG, Renzaglia KS. 1993. The gametophyte-sporophyte junction in land plants. In Advances in Botanical Research, Vol. 19, pp. 231-318. Elsevier, Amsterdam.
133. Lokhorst GM, Star W. 1985. Ultrastructure of mitosis and cytokinesis in Klebsormidium Mucosum nov. comb., formerly Ulothrix Verrucosa (Chlorophyta). J Phycol 21: 466-476.
134. Lucas WJ, Lee J-Y. 2004. Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5: 712-726.
135. Mandoli DF. 1998. Elaboration of body plan and phase change during development of Acetabularia: How is the complex architecture of a giant unicell built? Annu Rev Plant Physiol Plant Mol Biol 49: 173-198.
136. Manton I, Ettl H. 1965.Observations on the fine structure of Mesostigma viride lauterborn. Bot J Linn Soc 59: 175-184.
137. Marchant HJ, Pickett Heaps JD. 1973. Mitosis and cytokinesis in Coleochaete scutata. J Phycol 9: 461-471.
138. Marin B, Melkonian M. 1999. Mesostigmatophyceae, a new class of streptophyte green algae revealed by SSU rRNA sequence comparisons. Protist 150: 399-417.
139. Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somerville C, Ralph J. 2009. Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Curr Biol 19: 169-175.
140. McCourt RM, Delwiche CF, Karol KG. 2004. Charophyte algae and land plant origins. Trends Ecol Evol (Amst) 19: 661-666.
141. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
142. Michod RE, Roze D. 2001. Cooperation and conflict in the evolution of multicellularity. Heredity 86: 1-7.
143. Miller SM, Kirk DL. 1999. glsA, a Volvox gene required for asymmetric division and germ cell specification, encodes a chaperone-like protein. Development 126: 649-658.
144. Mine I, Menzel D, Okuda K. 2008.Morphogenesis in giantcelled algae. Int Rev Cell Mol Biol 266: 37-83.
145. Nakada T, Misawa K, Nozaki H. 2008.Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol Phylogenet Evol 48: 281-291.
146. Nedelcu AM, Michod RE. 2006. The evolutionary origin of an altruistic gene. Mol Biol Evol 23: 1460-1464.
147. Nedelcu AM, Borza T, Lee RW. 2006. A land plant-specific multigene family in the unicellular Mesostigma argues for its close relationship to Streptophyta. Mol Biol Evol 23: 1011-1015.
148. Niklas KJ. 2000. The evolution of plant body plans—A biomechanical perspective. Ann Bot 85: 411-438.
149. Niklas KJ, Kutschera U. 2009. The evolution of the land plant life cycle. New Phytologist 185: 27-41.
150. Niklas KJ, Newman SA. 2013. The origins of multicellular organisms. Evol Dev 15: 41-52.
151. Niklas KJ, Cobb ED, Crawford DR. 2013. The evo-devo of multinucleate cells, tissues, and organisms, and an alternative route to multicellularity. Evol Dev 15: 466-474.
152. Nishii I. 2003. A kinesin, InvA, plays an essential role in Volvox morphogenesis. Cell 113: 743-753.
153. Nishii I, Miller SM. 2010. Volvox: Simple steps to developmental complexity? Curr Opin Plant Biol 13: 646-653.
154. Nishii I, Ogihara S. 1999. Actomyosin contraction of the posterior hemisphere is required for inversion of the Volvox embryo. Development 126: 2117-2127.
155. Nishimura Y, Shikanai T, Nakamura S, Kawai-Yamada M, Uchimiya H. 2012. Gsp1 triggers the sexual developmental program including inheritance of chloroplast DNA and mitochondrial DNA in Chlamydomonas reinhardtii. Plant Cell 24: 2401-2414.
156. Nozaki H. 1990. Ultrastructure of the extracellular matrix of Gonium (Volvocales, Chlorophyta)_. Phycologia 29: 1-8.
157. Nozaki H. 1996.Morphology and evolution of sexual reproduction in the Volvocaceae (Chlorophyta). J Plant Res 109: 353-361.
158. Nozaki H, Misawa K, Kajita T, Kato M, Nohara S, Watanabe MM. 2000. Origin and evolution of the colonial volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Mol Phylogenet Evol 17: 256-268.
159. Nozaki H, Mori T, Misumi O, Matsunaga S, Kuroiwa T. 2006a. Males evolved from the dominant isogametic mating type. Curr Biol 16: R1018-R1020.
160. Nozaki H, Ott FD, Coleman AW. 2006b. Morphology, molecular phylogeny and taxonomy of two new species of Pleodorina (Volvoceae, Chlorophyceae). J Phycol 42: 1072-1080.
161. Pandey S, Assmann SM. 2004. The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein asubunit GPA1 and regulates abscisic acid signaling. Plant Cell 16: 1616-1632.
162. Pappas V, Miller SM. 2009. Functional analysis of the Volvox carteri asymmetric division protein GlsA. Mech Dev 126: 842-851.
163. Parker GA, Baker RR, Smith VG. 1972. The origin and evolution of gamete dimorphism and the male-female phenomenon. J Theor Biol 36: 529-553.
164. Petersen J, Teich R, Becker B, Cerff R, Brinkmann H. 2006. The GapA/B gene duplication marks the origin of Streptophyta (charophytes and land plants). Mol Biol Evol 23: 1109-1118.
165. Pickett-Heaps JD. 1967. Ultrastructure and differentiation in Chara sp: II. Mitosis. Aust J Biol Sci 20: 883-894.
166. Pickett-Heaps JD. 1968. Ultrastructure and differentiation in Chara sp: III. Formation of the antheridium. Aust J Biol Sci 21: 255-274.
167. Pickett-Heaps JD. 1975. Green alage, structure, reproduction and evolution in selected genera. Sinauer, Sunderland, MA.
168. Pickett-Heaps J. 1976. Cell division in eucaryotic algae. Bio-Science 26: 445-450.
169. Pires ND, Dolan L. 2012. Morphological evolution in land plants: New designs with old genes. Philos Trans R Soc Lond B Biol Sci 367: 508-518.
170. Popper ZA, Michel G, Hervé C, Domozych DS, Willats WG., Tuohy MG, Kloareg B, Stengel DB. 2011. Evolution and diversity of plant cell walls: From algae to flowering plants. Annu Rev Plant Biol 62: 567-590.
171. Preston JC, Hileman LC, Cubas P. 2011. Reduce, reuse, and recycle: Developmental evolution of trait diversification. Am J Bot 98: 397-403.
172. Prigge MJ, Clark SE. 2006. Evolution of the class III HD-Zip gene family in land plants. Evol Dev 8: 350-361.
173. Prigge MJ, Lavy M, Ashton NW, Estelle M. 2010. Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr Biol 20: 1907-1912.
174. Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, et al. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329: 223-226.
175. Pröschold T, Marin B, Schlösser UG, Melkonian M. 2001. Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta): I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152: 265-300.
176. Pröschold T, Harris EH, Coleman AW. 2005. Portrait of a species: Chlamydomonas reinhardtii. Genetics 170: 1601-1610.
177. Proseus TE, Boyer JS. 2012. Pectate chemistry links cell expansion to wall deposition in Chara corallina. Plant Signal Behav 7: 1490-1492.
178. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogue F, Rameau C. 2011. Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539.
179. Queller DC. 2000. Relatedness and the fraternal major transitions. Philos Trans R Soc Lond B Biol Sci 355: 1647-1655.
180. Quodt V, Faigl W, Saedler H, Münster T. 2007. The MADSdomain protein PPM2 preferentially occurs in gametangia and sporophytes of the moss Physcomitrella patens. Gene 400: 25-34.
181. Randerson JP, Hurst LD. 2001. The uncertain evolution of the sexes. Trends Ecol Evol 16: 571-579.
182. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. Experimental evolution of multicellularity. Proc Natl Acad Sci 109: 1595-1600.
183. Ratcliff WC, Herron MD, Howell K, Pentz JT, Rosenzweig F, Travisano M. 2013. Experimental evolution of an alternating uni-and multicellular life cycle in Chlamydomonas reinhardtii. Nat Commun 4: 2742.
184. Raven JA. 1997. Miniview: Multiple origins of plasmodesmata. Eur J Phycol 32: 95-101.
185. Raven JA. 2013. Polar auxin transport in relation to longdistance transport of nutrients in the Charales. J Exp Bot 64: 1-9.
186. Rethy R. 1968. Red (R), far-red (FR) photoreversible effects on the growth of Chara sporelings. Z Pflanzenphysiol 59: 100-102.
187. Robaglia C, Menand B, Lei Y, Sormani R, Nicolaï M, Gery C, Teoulé E, Deprost D, Meyer C. 2004. Plant growth: The translational connection. Biochem Soc Trans 32: 581-584.
188. Rodriguez-Ezpeleta N, Philippe H, Brinkmann H, Becker B, Melkonian M. 2006. Phylogenetic analyses of nuclear, mitochondrial, and plastid multigene data sets support the placement of Mesostigma in the Streptophyta. Mol Biol Evol 24: 723-731.
189. Rokas A. 2008. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42: 235-251.
190. Ruyter-Spira C, Bouwmeester H. 2012. Strigolactones affect development in primitive plants. The missing link between plants and arbuscularmycorrhizal fungi? New Phytologist 195: 730-733.
191. Sabbatini MR, Argüello JA, Fernández OA, Bottini RA. 1987. Dormancy and growth-inhibitor levels in oospores of Chara contraria A. Braun ex Kütz. (Charophyta). Aquat Bot 28: 189-194.
192. Sakakibara K, Nishiyama T, Kato M, Hasebe M. 2001. Isolation of homeodomain-leucine zipper genes from the moss Physcomitrella patens and the evolution of homeodomain-leucine zipper genes in land plants. Mol Biol Evol 18: 491-502.
193. Sakakibara K, Ando S, Yip HK, Tamada Y, Hiwatashi Y, Murata T, Deguchi H, Hasebe M, Bowman JL. 2013. KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science 339: 1067-1070.
194. Sawa T, Frame PW. 1974. Comparative anatomy of Charophyta: I. Oogonia and oospores of Tolypella—With special reference to the sterile oogonial cell. Bull Torrey Bot Club 136-144.
195. Sawitzky H, Grolig F. 1995. Phragmoplast of the green alga Spirogyra is functionally distinct from the higher plant phragmoplast. J Cell Biol 130: 1359-1371.
196. Sebe-Pedros A, Irimia M, del Campo J, Parra-Acero H, Russ C, Nusbaum C, Blencowe BJ, Ruiz-Trillo I. 2013. Regulated aggregative multicellularity in a close unicellular relative of metazoa. Elife 2: e01287.
197. Sederias J, Colman B. 2007. The interaction of light and low temperature on breaking the dormancy of Chara vulgaris oospores. Aquat Bot 87: 229-234.
198. Sekimoto H, Abe J, Tsuchikane Y. 2012. New insights into the regulation of sexual reproduction in Closterium. Int Rev Cell Mol Biol 297: 309-338.
199. Šetlík I, Zachleder V. 1984. The multiple fission cell reproductive patterns in algae. In The microbial cell cycle (ed. Nurse P, Streiblová E), pp. 253-279. CRC, Boca Raton, FL.
200. Shikano S, Luckinbill LS, Kurihara Y. 1990. Changes of traits in a bacterial population associated with protozoal predation. Microb Ecol 20: 75-84.
201. Simon A, Glöckner G, Felder M, Melkonian M, Becker B. 2006. ESTanalysis of the scaly green flagellateMesostigma viride (Streptophyta): Implications for the evolution of green plants (Viridiplantae). BMC Plant Biol 6: 2.
202. Singer SD, Krogan NT, Ashton NW. 2007. Clues about the ancestral roles of plant MADS-box genes from a functional analysis of moss homologues. Plant Cell Rep 26: 1155-1169.
203. Smaczniak C, Immink RGH, Angenent GC, Kaufmann K. 2012. Developmental and evolutionary diversity of plant MADS-domain factors: Insights from recent studies. Development 139: 3081-3098.
204. Smolarkiewicz M, Dhonukshe P. 2013. Formative cell divisions: Principal determinants of plant morphogenesis. Plant Cell Physiol 54: 333-342.
205. Solnica-Krezel L, Sepich DS. 2012. Gastrulation: Making and shaping germ layers. Annu Rev Cell Dev Biol 28: 687-717.
206. Sørensen I, Domozych D, Willats WGT. 2010. How have plant cell walls evolved? Plant Physiol 153: 366-372.
207. Sørensen I, Pettolino FA, Bacic A, Ralph J, Lu F, O’Neill MA, Fei Z, Rose JKC, Domozych DS, Willats WGT. 2011. The charophycean green algae provide insights into the early origins of plant cell walls. Plant J 68: 201-211.
208. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720-726.
209. Stanley SM. 1973. An ecological theory for the sudden origin of multicellular life in the late precambrian. ProcNatl Acad Sci 70: 1486-1489.
210. Stark K, Kirk D., Schmitt R. 2001. Two enhancers and one silencer located in the introns of regA control somatic cell differentiation in Volvox carteri. Genes Dev 15: 1449-1460.
211. Starr RC. 1970. Control of differentiation in Volvox. Symp Soc Dev Biol 29: 59-100.
212. Stebbins GL, Hill G. 1980. Did multicellular plants invade the land? Am Nat 115: 342-353.
213. Stewart KD, Mattox KR. 1975. Comparative cytology, evolution and classification of the green algae with some consideration of the origin of other organisms with chlorophylls a and b. Botan Rev 41: 104-135.
214. Stirk WA, Bálint P, Tarkowská D, Novák O, Strnad M, Ördög V, van Staden J. 2013a. Hormone profiles in microalgae: Gibberellins and brassinosteroids. Plant Physiol Biochem 70: 348-353.
215. Stirk WA, Ö rdög V, Novák O, Rolčík J, Strnad M, Bálint P, van Staden J. 2013b. Auxin and cytokinin relationships in 24 microalgal strains 1. J Phycol 49: 459-467.
216. Szathmáry E, Smith JM. 1995. The major evolutionary transitions. Nature 374: 227-232.
217. Sztein AE, Cohen JD, Cooke TJ. 2000. Evolutionary patterns in the auxin metabolism of green plants. Int J Plant Sci 161: 849-859.
218. Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Münster T, Theissen G, Nozaki H, Ito M. 2005. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci 102: 2436-2441.
219. Tarakhovskaya ER, Maslov YI, Shishova MF. 2007. Phytohormones in algae. Russ J Plant Physiol 54: 163-170.
220. Timme RE, Bachvaroff TR, Delwiche CF. 2012. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7: e29696.
221. Timme RE, Delwiche CF. 2010.Uncovering the evolutionary origin of plant molecular processes: Comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biol 10: 96.
222. Tsekos I. 1999. The sites of cellulose synthesis in algae: Diversity and evolution of cellulose-synthesizing enzyme complexes. J Phycol 35: 635-655.
223. Turmel M, Ehara M, Otis C, Lemieux C. 2002. Phylogenetic relationships among streptophytes as inferred from chloroplast small and large subunit rRNA gene sequences. J Phycol 38: 364-375.
224. Ueki N, Nishii I. 2008. Idaten is a new cold-inducible transposon of Volvox carteri that can be used for tagging developmentally important genes. Genetics 180: 1343-1353.
225. Ueki N, Nishii I. 2009. Controlled enlargement of the glycoprotein vesicle surrounding a Volvox embryo requires the InvB nucleotide-sugar transporter and is required for normal morphogenesis. Plant Cell 21: 1166-1181.
226. Ueki N, Matsunaga S, Inouye I, Hallmann A. 2010. How 5000 independent rowers coordinate their strokes in order to row into the sunlight: Phototaxis in the multicellular green alga Volvox. BMC Biol 8: 1-21.
227. Umen JG. 2005. The elusive sizer. Curr Opin Cell Biol 17: 435-441.
228. Umen JG. 2011. Evolution of sex and mating loci: An expanded view from Volvocine algae. Curr Opin Microbiol 14: 634-641.
229. Umen JG, Goodenough UW. 2001. Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Genes Dev 15: 1652-1661.
230. Umen JG, Olson BJSC. 2012. Genomics of volvocine algae. In Genomic insights into the biology of algae (ed. Piganeau G), Vol. 64, pp. 185-243. Elsevier, Amsterdam.
231. Vandenbussche F, Fierro AC, Wiedemann G, Reski R, Van Der Straeten D. 2007. Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Biol 7: 65.
232. Vannerum K, Huysman MJJ, De Rycke R, Vuylsteke M, Leliaert F, Pollier J, Lütz-Meindl U, Gillard J, De Veylder L, Goossens A, et al. 2011. Transcriptional analysis of cell growth and morphogenesis in the unicellular green alga Micrasterias (Streptophyta), with emphasis on the role of expansin. BMC Plant Biol 11: 128.
233. Van Sandt VST, Stieperaere H, Guisez Y, Verbelen J-P, Vissenberg K. 2007. XET activity is found near sites of growth and cell elongation in bryophytes and some green algae:New insights into the evolution of primary cellwall elongation. Ann Bot 99: 39-51.
234. Viamontes G, Kirk D. 1977. Cell shape changes and the mechanism of inversion in Volvox. J Cell Biol 75: 719-730.
235. Wallace S, Fleming A, Wellman CH, Beerling DJ. 2011. Evolutionary development of the plant spore and pollenwall. AoB Plants 2011: plr027.
236. Wang W, Esch JJ, Shiu S-H, Agula H, Binder BM, Chang C, Patterson SE, Bleecker AB. 2006. Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell 18: 3429-3442.
237. Waters ER. 2003. Molecular adaptation and the origin of land plants. Mol Phylogenet Evol 29: 456-463.
238. Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B. 2011. Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11: 104.
239. Zalewski CS, Floyd SK, Furumizu C, Sakakibara K, Stevenson DW, Bowman JL. 2013. Evolution of the class IV HDZip gene family in streptophytes. Mol Biol Evol 30: 2347-2365.
240. Zhong B, Liu L, Yan Z, Penny D. 2013. Origin of land plants using the multispecies coalescent model. Trends Plant Sci 18: 492-495.
241. Zobell O, Faigl W, Saedler H, Munster T. 2010. MIKC_MADS-Box proteins: Conserved regulators of the gametophytic generation of land plants. Mol Biol Evol 27: 1201-1211.