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Phylogenetic Analysis of GRAS Proteins from Moss, Lycophyte And ARTICLE ADDENDUM Plant Signaling & Behavior 6:6, 1-5; June 2011; © 2011 Landes Bioscience Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants Eric M. Engstrom Biology Department; The College of William and Mary; Williamsburg, VA USA RAS genes are a large family of Improved GRAS Protein Gstreptophyte specific transcription Phylogenies May Predict Cellular factors that function in a diverse set of HAM Protein Functions physiological and developmental pro- cesses. GRAS proteins of the HAIRY The Petunia HAIRY MERISTEM MERISTEM (HAM) sub-family are (HAM) protein, a member of the GRAS required for maintenance of shoot and family of transcription factors, was first root indeterminacy. The transcriptional identified as a component of a novel signal- targets of HAM proteins and the signal- ing pathway in Petunia, promoting shoot ing inputs regulating HAM activity are indeterminacy.1 Petunia ham mutants completely unknown. Understanding exhibit a novel phenotype of cessation of the relationship of HAM proteins to organogenesis (meristem arrest) followed other members of the GRAS family may by or simultaneous with differentiation of inform hypotheses relating to cellular the meristem as stem tissue. Three inde- level HAM functions. I here report a pendent studies have recently extended phylogenetic analysis of GRAS proteins analysis of HAM function from Petunia employing the complete set of known into Arabidopsis.2-4 My laboratory, in col- and probable GRAS proteins from the laboration with Dr. Rossangela Sozzani, sequenced genomes of the flowering recently described the phenotypes of Key words: GRAS, transcription factor, plants Arabidopsis and Rice, the lyco- Arabidopsis ham1,2,3 and ham1,2,4 triple HAIRY MERISTEM, phylogenetics, phyte Selaginella moellendorffii, and loss-of-function mutants, demonstrating Selaginella, Physcomitrella, land plant the bryophyte Physcomitrella patens. that AtHAMs are required for mainte- evolution HAM proteins are most closely related nance of indeterminacy in the root as well Submitted: 02/16/11 to DELLA proteins, key components as the shoot, and that aspects of ham loss- of gibberellin perception. However, of-function phenotypes in both the shoot Accepted: 02/16/11 GRAS proteins diversified into a mini- and the root are attributable to altered 2 This manuscript has been published online, prior to printing. Once the issue is complete and page numbers have been assigned, the citation will change accordingly. the issue is complete and page numbers have Once to printing. has been published online, prior This manuscript DOI: 10.4161/psb.6.6.15203 mum of 12 discreet monophyletic lin- regulation of cell-division. Correspondence to: Eric M. Engstrom; eages, including the HAM and DELLA Beyond a probable function as tran- Email: [email protected] subfamilies, prior to divergence of the scription factors,3,5 cellular-level functions moss and flowering plant lineages. of HAM proteins are entirely unknown. Addendum to: Engstrom EM, Andersen CM, Substantial diversification of GRAS Direct transcriptional targets of HAM Gumulak-Smith J, Hu J, Orlova E, Sozzani R, proteins at so early a point in land plant proteins, as well as proteins or other fac- Bowman JL. Arabidopsis homologs of the evolution suggests that relative related- tors that directly interact with HAM pro- Petunia HAIRY MERISTEM gene are required for maintenance of shoot and root indeterminacy. ness among GRAS protein sub-families teins, remain to be identified. Hypotheses Plant Physiol 2011; 155:735–50; PMID: 21173022; may not substantially reflect shared for testing cellular-level HAM functions DOI: 10.1104/pp.110.16875. protein function. may be informed by our understanding www.landesbioscience.com Plant Signaling & Behavior 1 of the transcriptional targets and cellu- of the moss Physcomitrella patens and the Substantial expansion of GRAS genes lar interactions of related GRAS proteins lycophyte Selaginella moellendorffii, in has occurred within specific GRAS sub- that are understood to some detail.2 As the order to gauge the extent of GRAS and families in a manner specific both to the likelihood for shared function may corre- HAM protein antiquity. particular GRAS subfamily and to the late with the degree of relatedness, efforts Bayesian analysis of 174 GRAS proteins, particular taxa analyzed, suggesting that to expand our understanding of HAM including the complete or near-complete GRAS genes have been utilized extensively function provides impetus for under- set of GRAS-proteins from Arabidopsis in the evolutionary history of mosses, lyco- standing the phylogenetic relationship of thaliana, Oryza sativa, Selaginella moel- phytes and euphyllophytes, but in highly HAM proteins with other subfamilies of lendorffii and Physcomitrella patens, along lineage specific ways (Fig. 3). S. moellen- GRAS proteins. with selected GRAS proteins from other dorffii in particular appears to have relied GRAS proteins contribute to the regu- taxa that have been subjected to genetic or heavily upon the GRAS family during its lation of a diverse suite of physiological biochemical analyses of function,2,10,11,13,17-19 evolutionary history, as the S. moellendorf- and developmental processes, including and two GRAS proteins from the aquatic, fii genome contains more probable GRAS abiotic stress responses,6 phytochrome filamentous Streptophyte Spirogyra gener- encoding genes relative to genome size signal transduction,7 radial patterning,8,9 ated a phylogenetic tree, from which eight than P. patens, Rice or Arabidopsis. maintenance of organ indeterminacy,1,2 major GRAS protein subfamilies, des- Rooting the tree shown in Figure 1 shoot meristem initiation,10,11 gibberellin ignated Clades I–VIII, were designated would allow us to determine which clades signaling12 and nodulation.12 Genetic and based upon the earlier analyses of Bolle and associated functions are more basal biochemical characterization of GRAS and Tian and colleagues (Fig. 1, Sup. and which are more recently derived. protein function has been performed Fig. 1, Sup. Tab. 1, Sup. Methods). The Bolle’s analysis rooted GRAS proteins to date only in flowering plant species, phylogenetic tree in Figure 1 is largely with a metazoan STAT protein.15,23 This but homologs of flowering plant GRAS congruent with the earlier analysis of root is problematic, as the relationship genes have been identified in the lyco- Bolle.15 All of the major subfamilies of our between STAT and GRAS proteins, phyte Selaginella, demonstrating that the analysis are well supported, with poste- while plausible, remains uncertain and GRAS family predates divergence of the rior probabilities of 0.9 or greater, the sole the phylogenetic distance between GRAS lycophyte and euphyllophyte lineages.14 exception being Clade VIII with a pos- and STAT proteins may be too great for Given the impressive breadth of func- terior probability of 0.72. Though well- STAT proteins to function as meaningful tion displayed by GRAS proteins and supported, Clade IV, consisting solely of outgroups to GRAS proteins. We incor- their significance in regulating flowering three proteins, two from Rice and one porated Spirogyra GRAS proteins into plant development, questions of when from Selaginella, is perhaps artifactual, our analysis with the intent of rooting the and in what plant lineages specific classes the branch lengths indicating relatively GRAS family tree. Our results suggest of GRAS proteins arose, expanded and rapid rates of protein evolution, which that a GRAS protein from a Streptophyte acquired novel functions, is of consider- may have generated Clade IV as a result of lineage more basal than Spirogyra will be able interest within the broader contexts long-branch attraction.20 required to root GRAS proteins. To date of elucidating GRAS function and recon- The tree contains 12 well-supported we have failed to detect probable GRAS structing land plant evolution. monophyletic clades that include proteins homologs outside of the Streptophyte lin- from Physcomitrella, Selaginella and flow- eage in either the Chlamydomonas reinhar- Major GRAS Protein Subfamilies ering plants (Fig. 2), consistent with the dii or Ostreococcus genomes. Are Ancient common ancestor of the moss and vascu- The very ancient diversification of lar plant lineages possessing no fewer than GRAS proteins has implications for Earlier phylogenetic analyses of GRAS 12 GRAS genes. The presence of 12 or understanding the evolution of GRAS proteins, principally analyzing proteins more GRAS genes at such an early date, protein function, including possible cel- from Arabidopsis and Rice, define eight is consistent with either a rapid diversifica- lular-level functions of HAM proteins. major GRAS subfamilies largely congru- tion in GRAS genes shortly following the HAM proteins are most closely related to ent with the distinct functions of charac- transition of streptophytes to land or alter- DELLA proteins, both classes residing in terized GRAS proteins.15,16 However, the natively, with GRAS genes having under- GRAS Clade V. DELLAs are transcrip- analysis of Tian and colleagues does not gone substantial diversification in aquatic tional repressors of growth promoting resolve relationships among the major streptophytes preceding the transition to proteins whose activity is negatively regu- GRAS protein subfamilies, while that of
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