1932

Abstract

The life cycles of eukaryotes alternate between haploid and diploid phases, which are initiated by meiosis and gamete fusion, respectively. In both ascomycete and basidiomycete fungi and chlorophyte algae, the haploid-to-diploid transition is regulated by a pair of paralogous homeodomain protein encoding genes. That a common genetic program controls the haploid-to-diploid transition in phylogenetically disparate eukaryotic lineages suggests this may be the ancestral function for homeodomain proteins. Multicellularity has evolved independently in many eukaryotic lineages in either one or both phases of the life cycle. Organisms, such as land plants, exhibiting a life cycle whereby multicellular bodies develop in both the haploid and diploid phases are often referred to as possessing an alternation of generations. We review recent progress on understanding the genetic basis for the land plant alternation of generations and highlight the roles that homeodomain-encoding genes may have played in the evolution of complex multicellularity in this lineage.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120215-035227
2016-11-23
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/genet/50/1/annurev-genet-120215-035227.html?itemId=/content/journals/10.1146/annurev-genet-120215-035227&mimeType=html&fmt=ahah

Literature Cited

  1. Abe J, Hori S, Tsuchikane Y, Kitao N, Kato M, Sekimoto H. 1.  2011. Stable nuclear transformation of the Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol. 52:1676–85 [Google Scholar]
  2. Adl SM, Simpson AGB, Lane CE, Lukes J, Bass D. 2.  et al. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59:429–93 [Google Scholar]
  3. Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M. 3.  et al. 2012. AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139:3120–29 [Google Scholar]
  4. Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M. 4.  2008. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat. Genet. 40:1136–41 [Google Scholar]
  5. Barton MK, Poethig RS. 5.  1993. Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild-type and in the shoot meristemless mutant. Development 119:823–31 [Google Scholar]
  6. Bauer L. 6.  1956. Über vegetative sporogonbildung bei einer diploiden sippe von Georgia pellucida. Planta 46:604–18 [Google Scholar]
  7. Becker B, Marin B. 7.  2009. Streptophyte algae and the origin of embryophytes. Ann. Bot. 103:999–1004 [Google Scholar]
  8. Bellaoui M, Pidkowich MS, Samach A, Kushalappa K, Kohalmi SE. 8.  et al. 2001. The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell 13:2455–70 [Google Scholar]
  9. Bemer M, Grossniklaus U. 9.  2012. Dynamic regulation of Polycomb group activity during plant development. Curr. Opin. Plant Biol. 15:523–29 [Google Scholar]
  10. Bensaude M. 10.  1918. Recherches sur le cycle évolutif et la sexualité chez les Basidiomycétes Nemours, Fr.: H. Bouloy
  11. Berrie GK. 11.  1960. The chromosome numbers of liverworts (Hepaticae and Anthocerotae). Trans. Br. Bryol. Soc. 3:688–705 [Google Scholar]
  12. Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR. 12.  2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296:1858–60 [Google Scholar]
  13. Bharathan G, Janssen BJ, Kellogg EA, Sinha N. 13.  1997. Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa?. PNAS 94:13749–53 [Google Scholar]
  14. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H. 14.  et al. 2008. A conserved molecular framework for compound leaf development. Science 322:1835–39 [Google Scholar]
  15. Bower FO. 15.  1890. On antithetic as distinct from homologous alternation of generations in plants. Ann. Bot. 4:347–70 [Google Scholar]
  16. Bower FO. 16.  1908. Origin of a Land Flora: A Theory Based on the Facts of Alternation London: MacMillanLandmark work interpreting life cycle evolution in land plants as sterile elaborations of the sporophyte.
  17. Bowman JL. 17.  2013. Walkabout on the long branches of plant evolution. Curr. Opin. Plant Biol. 16:70–77 [Google Scholar]
  18. Brefeld O. 18.  1877. Botanische untersungungen über schimmelpilze. Heft III: Basidiomyceten I. Leipzig, Ger.: Arthur Felix
  19. Brizi U. 19.  1892. Appunti di teratologia briologica. Annu. Reale Ist. Bot. Roma 5:53–57 [Google Scholar]
  20. Bürglin TR. 20.  1997. Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res. 25:4173–80 [Google Scholar]
  21. Butenko Y, Ohad N. 21.  2011. Polycomb-group mediated epigenetic mechanisms through plant evolution. Biochim. Biophys. Acta 1809:395–406 [Google Scholar]
  22. Celakovsky L. 22.  1874. Ueber die verschiedenen Formen und die Bedeutung des Generationswechsels der Pflanzen. Sitzungsberichte Königl. Böhmischen Gesellschaft Wissensch. Prag. 2:21–61 [Google Scholar]
  23. Chamberlain CJ. 23.  1897. Life history of Lilium philadelphicum: the pollen grain. Bot. Gaz. 23:423–30 [Google Scholar]
  24. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH. 24.  et al. 2004. Interaction of polycomb-group proteins controlling flowering in Arabidopsis. Development 131:5263–76 [Google Scholar]
  25. Cock JM, Godfroy O, Macaisne N, Peters AF, Coelho SM. 25.  2014. Evolution and regulation of complex life cycles: a brown algal perspective. Curr. Opin. Plant Biol. 17:1–6 [Google Scholar]
  26. Cock JM, Sterck L, Rouze P, Scornet D, Allen AE. 26.  et al. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–21 [Google Scholar]
  27. Coelho SM, Godfroy O, Arun A, Corguillé GL, Petersd AF, Cock JM. 27.  2011. OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus. PNAS 108:11518–23Study reporting establishing Ectocarpus as a genetically tractable system and isolation of life cycle mutants. [Google Scholar]
  28. Collen J, Porcel B, Carre W, Ball SG, Chaparro C. 28.  et al. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. PNAS 110:5247–52 [Google Scholar]
  29. Darwin CF. 29.  1859. On the Origin of Species by Means of Natural Selection, or, The Preservation of Favoured Races in the Struggle for Life London: John Murray
  30. Delwiche CF, Cooper ED. 30.  2015. The evolutionary origin of a terrestrial flora. Curr. Biol. 25:R899–910 [Google Scholar]
  31. Derelle R, Lopez P, Le Guyader H, Manuel M. 31.  2007. Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol. Dev. 9:212–19 [Google Scholar]
  32. Ebersberger I, Simoes RD, Kupczok A, Gube M, Kothe E. 32.  et al. 2012. A consistent phylogenetic backbone for the fungi. Mol. Biol. Evol. 29:1319–34 [Google Scholar]
  33. Farlow WG. 33.  1874. An asexual growth from the prothallus of Pteris serrulata. Proc. Am. Acad. Sci. 9:68–73 [Google Scholar]
  34. Ferris PJ, Goodenough UW. 34.  1987. Transcription of novel genes, including a gene linked to the mating-type locus, induced by Chlamydomonas fertilization. Mol. Cell. Biol. 7:2360–66 [Google Scholar]
  35. Finet C, Timme RE, Delwiche CF, Marlétaz F. 35.  2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr. Biol. 20:2217–22 [Google Scholar]
  36. Finet C, Timme RE, Delwiche CF, Marlétaz F. 36.  2012. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr. Biol. 22:1456–57 [Google Scholar]
  37. Flores-Sandoval E, Eklund DM, Bowman JL. 37.  2015. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort Marchantia polymorpha. PLOS Genet. 11:e1005207 [Google Scholar]
  38. Floyd SK, Zalewski CS, Bowman JL. 38.  2006. Evolution of Class III homeodomain leucine zipper genes in streptophytes. Genetics 173:373–88 [Google Scholar]
  39. Freshwater DW, Fredericq S, Butler BS, Hommersand MH, Chase MW. 39.  1994. A gene phylogeny of the red algae (Rhodophyta) based on plastid rbcL. PNAS 91:7281–85 [Google Scholar]
  40. Furumizu C, Alvarez JP, Sakakibara K, Bowman JL. 40.  2015. Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication. PLOS Genet. 11:e1004980 [Google Scholar]
  41. Gillissen B, Bergemann J, Sandmann C, Schroeer B, Bolker M, Kahmann R. 41.  1992. A 2-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68:647–57 [Google Scholar]
  42. Goebel Kv. 42.  1926. Wilhelm Hofmeister. The Work and Life of a Nineteenth Century Botanist. London: Ray Soc.
  43. Goroschankin JN. 43.  1891. Beiträge zur kenntniss der morphologie und systematik der Chlamydomonaden. Bull. Soc. Imp. Nat. Moscou 5:101–42 [Google Scholar]
  44. Goutte C, Johnson AD. 44.  1988. A1-protein alters the DNA-binding specificity of α-2 repressor. Cell 52:875–82 [Google Scholar]
  45. Graham LE. 45.  1993. Origin of Land Plants New York: John Wiley & Sons
  46. Green JR. 46.  1909. A History of Botany 1860–1900 Being a Continuation of Sachs “History of Botany, 1530–1860.” Oxford: Clarendon Press [Google Scholar]
  47. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB. 47.  1998. Maternal control of embryogenesis by medea, a Polycomb group gene in Arabidopsis. Science 280:446–50 [Google Scholar]
  48. Guignard L. 48.  1899. Anthérozoïdes et la double copulation sexuelle chez les végétaux angiosperms. Revue Gén. Botanique 11:129–35 [Google Scholar]
  49. Hackbusch J, Richter K, Muller J, Salamini F, Uhrig JF. 49.  2005. A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. PNAS 102:4908–12 [Google Scholar]
  50. Haig D. 50.  2008. Homologous versus antithetic alternation of generations and the origin of sporophytes. Bot. Rev. 74:395–418 [Google Scholar]
  51. Hamant O, Pautot V. 51.  2010. Plant development: a TALE story. C. R. Biol. 333:371–81 [Google Scholar]
  52. Harholt J, Moestrup Ø, Peter U. 52.  2016. Why plants were terrestrial from the beginning. Trends Plant Sci. 21:96–101 [Google Scholar]
  53. Harvey WH. 53.  1858. Phycologia Australia; or, A History of Australian Seaweeds London: Lovell Reeve
  54. Hay A, Tsiantis M. 54.  2010. KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–65 [Google Scholar]
  55. Herskowitz I. 55.  1989. A regulatory hierarchy for cell specialization in yeast. Nature 342:749–57 [Google Scholar]
  56. Hofmeister W. 56.  1849. Die Entstehung des Embryo der Phanerogamen Leipzig: Friedrich Hofmeister
  57. Hofmeister W. 57.  1851. Vergleichende Untersuchungen der Keimung, Entfaltung und Fruchtbildung höherer Kryptogamen (Moose, Farne, Equisetaceen, Rhizokarpeen und Lykopodiaceen) und der Samenbildung der Coniferen Leipzig: Frederick Hofmeister57 and 58. Monumental work that proposed alternation of generations and united land plants as monophyletic clade.
  58. Hofmeister WFB. 58.  1862. On the Germination, Development, and Fructification of the Higher Cryptogamia, and on the Fructification of the Coniferae. London: Ray Soc50657 and 58. Monumental work that proposed alternation of generations and united land plants as monophyletic clade.
  59. Holzinger A, Kaplan F, Blaas K, Zechmann B, Komsic-Buchmann K, Becker B. 59.  2014. Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction. PLOS ONE 9:e110630 [Google Scholar]
  60. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N. 60.  et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978 [Google Scholar]
  61. Horst NA, Katz A, Pereman I, Decker EL, Ohad N, Reski R. 61.  2016. A single homeobox gene triggers phase transition, embryogenesis and asexual reproduction. Nat. Plants 2:15209Demonstrated that ectopic TALE-HD expression induced transition from gametophyte to sporophyte in Physcomitrella. [Google Scholar]
  62. Hull CM, Boily MJ, Heitman J. 62.  2005. Sex-specific homeodomain proteins Sxi1 alpha and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot. Cell 4:526–35 [Google Scholar]
  63. Ju C, Van de Poel B, Cooper ED, Theirer JH, Gibbons TR. 63.  et al. 2015. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants 1:14004 [Google Scholar]
  64. Kamada T. 64.  2002. Molecular genetics of sexual development in the mushroom Coprinus cinereus. BioEssays 24:449–59 [Google Scholar]
  65. Karol KG, McCourt RM, Cimino MT, Delwiche CF. 65.  2001. The closest living relative of plants. Science 294:2351–53 [Google Scholar]
  66. Kato H, Ishizaki K, Kouno M, Shirakawa M, Bowman JL. 66.  et al. 2015. Auxin-mediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha. PLOS Genet. 11:e1005084 [Google Scholar]
  67. Katz A, Oliva M, Mosquna A, Hakim O, Ohad N. 67.  2004. FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J. 37:707–19 [Google Scholar]
  68. Kerstetter RA, Laudencia-Chingcuanco D, Smith LG, Hake S. 68.  1997. Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development 124:3045–54 [Google Scholar]
  69. King N, Westbrook MJ, Young SL, Kuo A, Abedin M. 69.  et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–88 [Google Scholar]
  70. Knoll AH. 70.  2011. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39:217–39 [Google Scholar]
  71. Kues U, Richardson WVJ, Tymon AM, Mutasa ES, Gottgens B. 71.  et al. 1992. The combination of dissimilar alleles of the A alpha and A beta gene complexes, whose proteins contain homeo domain motifs, determines sexual development in the mushroom Coprinus cinereus. Genes Dev. 6:568–77 [Google Scholar]
  72. Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S. 72.  et al. 2007. The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19:2719–35 [Google Scholar]
  73. Kylin H. 73.  1935. Remarks on the life-history of the Rhodophyceae. Bot. Rev. 1:138–48 [Google Scholar]
  74. Lang WH. 74.  1901. On apospory in Anthoceros laevis. Ann. Bot. 10:503–10 [Google Scholar]
  75. Laurin-Lemay S, Brinkmann H, Philippe H. 75.  2012. Origin of land plants revisited in the light of sequence contamination and missing data. Curr. Biol. 22:R593–94 [Google Scholar]
  76. Lee J-H, Lin H, Joo S, Goodenough U. 76.  2008. Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133:829–40Seminal work elucidating that the haploid-to-diploid transition in Chlamydomonas is regulated by a BELL-KNOX heterodimer. [Google Scholar]
  77. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H. 77.  et al. 2012. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31:1–46 [Google Scholar]
  78. Levin TC, King N. 78.  2013. Evidence for sex and recombination in the choanoflagellate Salpingoeca rosetta. Curr. Biol. 23:2176–80 [Google Scholar]
  79. Lewis LA, McCourt RM. 79.  2004. Green algae and the origin of land plants. Am. J. Bot. 91:1535–56 [Google Scholar]
  80. Li EY, Bhargava A, Qiang WY, Friedmann MC, Forneris N. 80.  et al. 2012. The Class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus. New Phytol. 194:102–15 [Google Scholar]
  81. Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S. 81.  1994. A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6:1859–76 [Google Scholar]
  82. Lodha M, Marco CF, Timmermans MCP. 82.  2013. The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev. 27:596–601 [Google Scholar]
  83. Long JA, Moan EI, Medford JI, Barton MK. 83.  1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69 [Google Scholar]
  84. Marchal É, Marchal É. 84.  1907. Aposporie et sexualité chez les Mousses I. Bull. Acad. R. Sci. Belg. Cl. Sci. 1907:65–89 [Google Scholar]
  85. Marchal É, Marchal É. 85.  1909. Aposporie et sexualité chez les Mousses II. Bull. Acad. R. Sci. Belg. Cl. Sci. 1909:1249–88 [Google Scholar]
  86. Marchal É, Marchal É. 86.  1911. Aposporie et sexualité chez les Mousses III. Bull. Acad. R. Sci. Belg. Cl. Sci. 1911:750–88 [Google Scholar]
  87. Marchant J. 87.  1713. Nouvelle Découverte des fleurs et des graines D'une Plante rangée par les Botanistes fous le genre du Lichen. Histoire de l'Académie royale des sciences, avec les mémoires de mathématique et de physique, pour la meme cette Académie. Année 1713:229–34 [Google Scholar]
  88. Matsuzaki M, Misumi O, Shin–I T, Maruyama S, Takahara M. 88.  et al. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–57 [Google Scholar]
  89. Matzke EB, Raudzens L. 89.  1968. Aposporous diploid gametophytes from sporophytes of the liverwort Blasia pusilla L. PNAS 58:752–55 [Google Scholar]
  90. Mele G, Ori N, Sato Y, Hake S. 90.  2003. The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev. 17:2088–93 [Google Scholar]
  91. Menand B, Yi KK, Jouannic S, Hoffmann L, Ryan E. 91.  et al. 2007. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316:1477–80 [Google Scholar]
  92. Mirbel C-F. 92.  1835. Researches anatomiques et physiologiques sur le Marchantia polymorpha. Mém. Acad. R. Sci. Inst. France 13:337–436 [Google Scholar]
  93. Mosquna A, Katz A, Decker EL, Rensing SA, Reski R, Ohad N. 93.  2009. Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136:2433–4493 and 97. Studies describing PRC2-mediated repression of sporophyte body development during the gametophyte generation in Physcomitrella. [Google Scholar]
  94. Niklas KJ, Newman SA. 94.  2013. The origins of multicellular organisms. Evol. Dev. 15:41–52 [Google Scholar]
  95. Nishimura Y, Shikanai T, Nakamura S, Kawai–Yamada M, Uchimiya H. 95.  2012. Gsp1 triggers the sexual developmental program including inheritance of chloroplast DNA and mitochondrial DNA in Chlamydomonas reinhardtii. Plant Cell 24:2401–14 [Google Scholar]
  96. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D. 96.  et al. 1999. Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11:407–15 [Google Scholar]
  97. Okano Y, Aonoa N, Hiwatashia Y, Murata T, Nishiyama T. 97.  et al. 2009. A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. PNAS 106:16321–2693 and 97. Studies describing PRC2-mediated repression of sporophyte body development during the gametophyte generation in Physcomitrella. [Google Scholar]
  98. Oltmanns F. 98.  1898. Die Entwickelung der Sexualorgane bei Coleochaete pulvinata. Flora 85:1–14 [Google Scholar]
  99. Overton E. 99.  1893. On the reduction of the chromosomes in the nuclei of plants. Ann. Bot. 7:139–43 [Google Scholar]
  100. Pagnussat GC, Yu HJ, Sundaresana V. 100.  2007. Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell 19:3578–92 [Google Scholar]
  101. Pires ND, Yi KK, Breuninger H, Catarino B, Menand B, Dolan L. 101.  2013. Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. PNAS 110:9571–76 [Google Scholar]
  102. Pringsheim N. 102.  1860. Beiträge zur Morphologie und Systematik der Algen III Die Coleochaeteen. Jahrb. Wiss. Botanik 2:1–38 [Google Scholar]
  103. Pringsheim N. 103.  1876. Über vegetative Sprossung der Moosfrüchte. Monatsberichte Köneiglich Preussisched Akad. Wissensch. zu Berlin 1876:425–30 [Google Scholar]
  104. Pringsheim N. 104.  1878. Ueber Sprossung der Moosfrüchte und den Generationswechsel der Thallophyten. Jahrb. Wiss. Botanik 11:1–46 [Google Scholar]
  105. Ragan MA, Bird CJ, Rice EL, Gutell RR, Murphy CA, Singh RK. 105.  1994. A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit ribosomal-RNA gene. PNAS 91:7276–80 [Google Scholar]
  106. Sakakibara K, Ando S, Yip HK, Tamada Y, Hiwatashi Y. 106.  et al. 2013. KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science 339:1067–70Study demonstrating that KNOX2 genes repress the gametophytic developmental program during the sporophyte generation in Physcomitrella. [Google Scholar]
  107. Sakakibara K, Nishiyama T, Deguchi H, Hasebe M. 107.  2008. Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol. Dev. 10:555–66 [Google Scholar]
  108. Sakakibara K, Reisewitz P, Aoyama T, Friedrich T, Ando S. 108.  et al. 2014. WOX13-like genes are required for reprogramming of leaf and protoplast cells into stem cells in the moss Physcomitrella patens. Development 141:1660–70 [Google Scholar]
  109. Schwarzenbach M. 109.  1926. Regeneration and Aprosporie bei Anthoceros. Arch. Julius Klaus-Stiftung Vererb. 2:91–141 [Google Scholar]
  110. Searles RB. 110.  1980. The strategy of the red algal life history. Am. Nat. 115:113–20 [Google Scholar]
  111. Serikawa KA, Martinez-Laborda A, Kim HS, Zambryski PC. 111.  1997. Localization of expression of KNAT3, a class 2 knotted1-like gene. Plant J. 11:853–61 [Google Scholar]
  112. Singer SD, Ashton NW. 112.  2007. Revelation of ancestral roles of KNOX genes by a functional analysis of Physcomitrella homologues. Plant Cell Rep. 26:2039–54 [Google Scholar]
  113. Smith GM. 113.  1938. Nuclear phases and alternation of generations in the Chlorophyceae. Bot. Rev. 4:132–39 [Google Scholar]
  114. Smith GM. 114.  1955. Cryptogamic Botany, Vol. 1: Algae and Fungi. New York: McGraw–Hill399
  115. Smith HMS, Boschke I, Hake S. 115.  2002. Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. PNAS 99:9579–84 [Google Scholar]
  116. Sørensen I, Fei ZJ, Andreas A, Willats WGT, Domozych DS, Rose JKC. 116.  2014. Stable transformation and reverse genetic analysis of Penium margaritaceum: a platform for studies of charophyte green algae, the immediate ancestors of land plants. Plant J. 77:339–51 [Google Scholar]
  117. Spit A, Hyland RH, Mellor EJC, Casselton LA. 117.  1998. A role for heterodimerization in nuclear localization of a homeodomain protein. PNAS 95:6228–33 [Google Scholar]
  118. Stebbins GL, Hill GJC. 118.  1980. Did multicellular plants invade the land?. Am. Nat. 115:342–53 [Google Scholar]
  119. Strasburger E. 119.  1894. Über periodische Reducktion der Chromosomenzahl im Entwicklungsgang der Organismen. Ann. Bot. 8:281–316 [Google Scholar]
  120. Strasburger E. 120.  1906. Typische und allotypische Kernteilung. Ergebnisse und Erörterungen. Jahrb. Wiss. Botanik 42:1–71 [Google Scholar]
  121. Svedelius N. 121.  1931. Nuclear phases and alternation in the Rhodophyceae. Beih. Bot. Centralbl. 48:38–59 [Google Scholar]
  122. Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M. 122.  et al. 2005. Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. PNAS 102:2436–41 [Google Scholar]
  123. Taylor WR. 123.  1936. Phaeophycean life-histories in relation to classification. Bot. Rev. 2:554–63 [Google Scholar]
  124. Thuret G. 124.  1851. Recherches sur les Zoospores des Algues et les Anthéridies des Cryptogames. Ann. Sci. Nat. Bot. 3.16:5–39 [Google Scholar]
  125. Timme RE, Bachvaroff TR, Delwiche CF. 125.  2012. Broad phylogenomic sampling and the sister lineage of land plants. PLOS ONE 7:e29696 [Google Scholar]
  126. Timme RE, Delwiche CF. 126.  2010. Uncovering the evolutionary origin of plant molecular processes: comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biol. 10:96 [Google Scholar]
  127. Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J. 127.  2006. A map of KNAT gene expression in the Arabidopsis root. Plant Mol. Biol. 60:1–20 [Google Scholar]
  128. Umen JG. 128.  2014. Green algae and the origins of multicellularity in the plant kingdom. Cold Spring Harb. Perspect. Biol. 6:a016170 [Google Scholar]
  129. Unger F. 129.  1837. Weitere Beobachtungen über die Samenthiere der Pflanzen. Nova Acta Phys. Med. ACL 18:786–96 [Google Scholar]
  130. Urban M, Kahmann R, Bolker M. 130.  1996. Identification of the pheromone response element in Ustilago maydis. Mol. Gen. Genet. 251:31–37 [Google Scholar]
  131. Vaizey JR. 131.  1890. Alternation of generations in green plants. Ann. Bot. 4:371–78 [Google Scholar]
  132. Vollbrecht E, Veit B, Sinha N, Hake S. 132.  1991. The developmental gene knotted-1 is a member of a maize homeobox gene family. Nature 350:241–43 [Google Scholar]
  133. Weinmann JW, Bieler AK, Dieterichs JGN, Haid JJ, Ridinger JE. 133.  et al. 1737–1745. Phytanthoza Iconographia Regensburg: Hieronymum Lentzium
  134. Wellman CH, Strother PK. 134.  2015. The terrestrial biota prior to the origin of land plants (Embryophytes): a review of the evidence. Palaeontology 58:601–27 [Google Scholar]
  135. Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E. 135.  et al. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS 111:E4859–68 [Google Scholar]
  136. Wodniok S, Brinkmann H, Glockner G, Heidel AJ, Philippe H. 136.  et al. 2011. Origin of land plants: Do conjugating green algae hold the key?. BMC Evol. Biol. 11:104 [Google Scholar]
  137. Wylie AP. 137.  1957. Chromosome numbers of mosses. Trans. Br. Bryol. Soc. 2:260–78 [Google Scholar]
  138. Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M. 138.  et al. 2014. Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Science 343:1505–8 [Google Scholar]
  139. Xu L, Shen WH. 139.  2008. Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr. Biol. 18:1966–71 [Google Scholar]
  140. Yamanouchi S. 140.  1906. The life history of Polysiphonia violacea. Bot. Gaz. 42:401–49 [Google Scholar]
  141. Yamanouchi S. 141.  1906. The life history of Polysiphonia violacea. Bot. Gaz. 41:425–33 [Google Scholar]
  142. Yip HK, Floyd SK, Sakakibara K, Bowman JL. 142.  2016. Class III HD-Zip activity coordinates leaf development in Physcomitrella patens. Dev. Biol. doi: 10.1016/j.ydbio.2016.01.012
  143. Zhao H, Lu M, Singh R, Snell WJ. 143.  2001. Ectopic expression of a Chlamydomonas mt+-specific homeodomain protein in mt− gametes initiates zygote development without gamete fusion. Genes Dev. 15:2767–77 [Google Scholar]
  144. Zhong RQ, Lee CH, Zhou JL, McCarthy RL, Ye ZH. 144.  2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–82 [Google Scholar]
/content/journals/10.1146/annurev-genet-120215-035227
Loading
/content/journals/10.1146/annurev-genet-120215-035227
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error