Phylogenomic synteny network analyses reveal ancestral transpositions of auxin response factor genes in plants

Authors: GAO, BEI - The Chinese University Of Hong Kong (CUHK); WANG, LIUQIANG - The Chinese University Of Hong Kong (CUHK); Oliver, Melvin; CHEN, MOXIAN - The Chinese University Of Hong Kong (CUHK); ZHANG, JIANHUA - Hong Kong Baptist University

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/30/2020
Publication Date: 5/14/2020
Citation: Gao, B., Wang, L., Oliver, M.J., Chen, M., Zhang, J. 2020. Phylogenomic synteny network analyses reveal ancestral transpositions of auxin response factor genes in plants. BMC Plant Biology. 16: Article 70. https://doi.org/10.1186/s13007-020-00609-1.
DOI: https://doi.org/10.1186/s13007-020-00609-1

Interpretive Summary: The plant hormone auxin, the chemically simple molecule (indole-3-acetic acid [IAA]), controls many physiological and developmental processes in plants including most of the attributes in crops that impact productivity and yield. Auxin response factors (ARFs), that mediate the auxin control of plant development, have long been a research focus as potential keys for manipulation of plant growth for crop improvement. ARF genes occur in all plant lineages and each plant has a large family of ARF genes that play various roles in plant development and other processes. To fully understand the roles that ARFs play in plant development it is necessary to understand how these genes evolved through the history of land plants and how each member of the family arose and functions within any of the wide diversity of plants, incuding crops. In this study we collected the DNA sequences of over 3,500 ARF genes collected from as many plants as were available in the public databases. From these genes we constructed a large and accurate phylogeny (a gene family tree) and using the DNA sequences that surround these genes we could uncover how each gene in the ARF gene family evolved throughout the phylogeny. Using a new network analysis protocol, we could identify when genes appeared from gene duplication events and also when they were moved within the genomes of the plants to change their functionality. The analysis allows us to unravel the role that the ARF genes play the evolution of the complex vegetative changes that shape the modern plants we now cultivate for food. This knowledge enables us to predict, from the natural “experiment” that is evolution, how we might manipulate ARF genes to improve crop productivity and yield.

Technical Abstract: Background Auxin response factors (ARFs) have long been a research focus and represent a class of key regulators of plant growth and development. Integrated phylogenomic synteny network analyses were able to provide novel insights into the evolution of the ARF gene family. Results Here, more than 3500 ARFs collected from plant genomes and transcriptomes covering major streptophyte lineages were used to reconstruct the broad-scale family phylogeny, where the early origin and diversification of ARF in charophytes was delineated. Based on the family phylogeny, we proposed a unified six-group classification system for angiosperm ARFs. Phylogenomic synteny network analyses revealed the deeply conserved genomic syntenies within each of the six ARF groups and the interlocking syntenic relationships connecting distinct groups. Recurrent duplication events, such as those that occurred in seed plants, angiosperms, core eudicots and grasses contributed to the expansion of ARF genes which facilitated functional diversification. Ancestral transposition activities in important plant families, including crucifers, legumes and grasses, were unveiled by synteny network analyses. Ancestral gene duplications along with transpositions have profound evolutionary significance which may have accelerated the functional diversification process of paralogues. Conclusions The broad-scale family phylogeny in combination with the state-of-art phylogenomic synteny network analyses not only allowed us to infer the evolutionary trajectory of ARF genes across distinct plant lineages, but also facilitated to generate a more robust classification regime for this transcription factor family. Our study provides insights into the evolution of ARFs which will enhance our current understanding of this important transcription factor family.