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Genome-wide Comparative Analysis of the GRAS Gene Family in Populus, Arabidopsis and Rice

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Abstract

GRAS genes belong to a gene family of transcription regulators that function in the regulation of plant growth and development. Our knowledge about the expansion and diversification of this gene family in flowering plants is presently limited to the herbaceous species Arabidopsis and rice. Numerous aspects, including the phylogenetic history, expansion, functional divergence and adaptive evolution await further study, especially in woody tree species. Based on the latest genome assemblies, we found 106, 34 and 60 putative GRAS genes in Populus, Arabidopsis and rice, respectively. Phylogenetic analysis revealed that GRAS proteins could be divided into at least 13 subfamilies. Tandem and segmental duplications are the most common expansion mechanisms of this gene family, and their frequent joint action may explain the rapid expansion in Populus. Site-specific shifts in evolutionary rates might be the main force driving subfamily-specific functional diversification. Adaptive evolution analysis revealed that GRAS genes have evolved mainly under purifying selection after duplication, suggesting that strong functional constraints have a bearing on the evolution of GRAS genes. Both expressed sequence tags (EST) and microarray data revealed that GRAS genes in Populus have broad expression patterns across a variety of organs/tissues. Expression divergence analyses between paralogous pairs of GRAS genes suggested that the retention of GRAS genes after duplication could be mainly attributed to substantial functional novelty such as neo-functionalization or sub-functionalization. Our study highlights the expansion and diversification of the GRAS gene family in Populus and provides the first comprehensive analysis of this gene family in the Populus genome.

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Acknowledgements

We thank Dr. Stefan Zoller from the Genetic Diversity Center, ETH Zürich, for bioinformatics support. We also thank Erin Gleeson and Matthew Scarborough for help with English writing. This work has been supported by China Scholarship Council (No. 2011491017).

Author Contributions

XL performed the data analysis, interpreted the results and drafted the manuscript. AW supervised the project and helped in drafting and revising the manuscript.

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  1. ETH Zürich, Institute of Integrative Biology, Universitätstrasse 16, Zurich, 8092, Switzerland

    Xuanyu Liu & Alex Widmer

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Correspondence to Xuanyu Liu.

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Fig. S1

Multiple sequence alignment of 176 GRAS domain sequences from Populus, Arabidopsis and rice. Conserved residues are shaded. The five conserved motifs within the domain (LHR I, VHIID, LHRII, PFYRE and SAM) are indicated above the sequence alignment following the study of Pysh et al. (1999) (PDF 575 kb)

Fig. S2

The maximum likelihood tree and Bayesian inference tree based on 176 GRAS proteins from Populus, Arabidopsis and rice. a The ML tree was generated using the PhyML 3.0 program (Guindon et al. 2010; Guindon and Gascuel 2003) with 100 bootstrap replicates, using BIONJ distance-based starting tree and under the JTT + I + G + F model as inferred by the program ProtTest 2.4 (Abascal et al. 2005). b Under the same model of evolution, MrBayes 3.2.1 program (Ronquist and Huelsenbeck 2003) was used to construct the Bayesian inference (BI) tree. Three independent runs were performed with four Markov chains starting from random trees, each consisting of 2 million generations with trees sampled every 1,000 generations (PDF 870 kb)

Fig. S3

Neighbor joining tree based on 176 full-length protein sequences of GRAS genes from Populus, Arabidopsis and rice (PDF 488 kb)

Fig. S4

Frequency and distribution of critical amino acid sites responsible for type I functional divergence between subfamilies along the GRAS domain. The five conserved motifs within the domain are indicated with colored boxes (PDF 281 kb)

Fig. S5

In silico expressed sequence tag (EST) analysis of Populus GRAS genes. EST frequency for each of the 39 Populus GRAS genes was counted by searching NCBI EST datasets from various libraries across a set of 18 organ/tissue types (PDF 673 kb)

Table S1

The GRAS genes identified in Arabidopsis, rice, Populus and other species. “ψ” prior to gene symbols indicates pseudogene fragments (XLS 129 kb)

Table S2

Tandem and segmental duplications of GRAS genes in Arabidopsis and rice. Genes in tandem clusters are indicated in red (XLS 53 kb)

Table S3

Type I functional divergence between subfamilies of GRAS genes (XLS 35 kb)

Table S4

Critical amino acid sites responsible for the type I functional divergence between subfamilies (XLS 43 kb)

Table S5

Sequence similarities, dN/dS ratios, and Pearson’s correlation coefficient of expression between paralogous genes in Arabidopsis, rice and Populus (XLS 111 kb)

Table S6

Likelihood ratio tests and parameter estimations for the six site models based on the coding sequences of 176 GRAS genes from Populus, Arabidopsis and rice (XLS 31 kb)

Table S7

Corresponding probe sets of Populus GRAS genes in Affymetrix microarray analysis (XLS 40 kb)

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Liu, X., Widmer, A. Genome-wide Comparative Analysis of the GRAS Gene Family in Populus, Arabidopsis and Rice. Plant Mol Biol Rep 32, 1129–1145 (2014). https://doi.org/10.1007/s11105-014-0721-5

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