Diversification of a Transcription Factor Family Led to the Evolution of Antagonistically Acting Genetic Regulators of Root Hair Growth

Abstract

Streptophytes colonized the land some time before 470 million years ago [1Clarke J.T. Warnock R.C.M. Donoghue P.C.J. Establishing a time-scale for plant evolution.New Phytol. 2011; 192: 266-301Crossref PubMed Scopus (250) Google Scholar, 2Bateman R.M. Crane P.R. DiMichele W.A. Kenrick P.R. Rowe N.P. Speck T. Stein W.E. Early evoltuion of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation.Annu. Rev. Ecol. Syst. 1998; 29: 263-292Crossref Scopus (242) Google Scholar, 3Wellman C.H. Osterloff P.L. Mohiuddin U. Fragments of the earliest land plants.Nature. 2003; 425: 282-285Crossref PubMed Scopus (422) Google Scholar]. The colonization coincided with an increase in morphological and cellular diversity [4Bowman J.L. Walkabout on the long branches of plant evolution.Curr. Opin. Plant Biol. 2013; 16: 70-77Crossref PubMed Scopus (67) Google Scholar, 5Dolan L. Body building on land: morphological evolution of land plants.Curr. Opin. Plant Biol. 2009; 12: 4-8Crossref PubMed Scopus (27) Google Scholar, 6Jones V.A.S. Dolan L. The evolution of root hairs and rhizoids.Ann. Bot. (Lond.). 2012; 110: 205-212Crossref PubMed Scopus (87) Google Scholar, 7Doyle J.A. Phylogenetic analyses and morphological evolution in land plants.in: Ambrose B.A. Purugganan M. Annual Plant Reviews Volume 45: The Evolution of Plant Form. John Wiley and Sons, 2013: 1-50Google Scholar]. This increase in diversity is correlated with a proliferation in transcription factors encoded in genomes [8Pires N. Dolan L. Early evolution of bHLH proteins in plants.Plant Signal. Behav. 2010; 5: 911-912Crossref PubMed Scopus (36) Google Scholar, 9Lang D. Weiche B. Timmerhaus G. Richardt S. Riaño-Pachón D.M. Corrêa L.G. Reski R. Mueller-Roeber B. Rensing S.A. Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity.Genome Biol. Evol. 2010; 2: 488-503Crossref PubMed Scopus (129) Google Scholar, 10Rensing S.A. Gene duplication as a driver of plant morphogenetic evolution.Curr. Opin. Plant Biol. 2014; 17: 43-48Crossref PubMed Scopus (141) Google Scholar]. This suggests that gene duplication and subsequent diversification of function was instrumental in the generation of land plant diversity. Here, we investigate the diversification of the streptophyte-specific Lotus japonicus ROOTHAIRLESS LIKE (LRL) transcription factor (TF) [11Karas B. Amyot L. Johansen C. Sato S. Tabata S. Kawaguchi M. Szczyglowski K. Conservation of lotus and Arabidopsis basic helix-loop-helix proteins reveals new players in root hair development.Plant Physiol. 2009; 151: 1175-1185Crossref PubMed Scopus (83) Google Scholar, 12Tam T.H.Y. Catarino B. Dolan L. Conserved regulatory mechanism controls the development of cells with rooting functions in land plants.Proc. Natl. Acad. Sci. USA. 2015; 112: E3959-E3968Crossref PubMed Scopus (62) Google Scholar] subfamily of basic loop helix (bHLH) proteins by comparing gene function in early divergent and derived land plant species. We report that the single Marchantia polymorpha LRL gene acts as a general growth regulator required for rhizoid development, a function that has been partially conserved throughout multicellular streptophytes. In contrast, the five relatively derived Arabidopsis thaliana LRL genes comprise two antagonistically acting groups of differentially expressed genes. The diversification of LRL genes accompanied the evolution of an antagonistic regulatory element controlling root hair development.