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Molecular Evolution and Local Root Heterogeneous Expression of the Chenopodium quinoa ARF Genes Provide Insights into the Adaptive Domestication of Crops in Complex Environments

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Abstract

Auxin response factors (ARFs) influence plant growth and development via the coupling of basic biological processes. However, the evolution, expansion, and regulatory mechanisms of ARFs in the domesticated crop quinoa after artificial selection remain elusive. In this study, we systematically identified 30 Chenopodium quinoa ARFs (CqARFs). In this typical domesticated crop, ARFs divided into three subfamilies are subjected to strong purification selection and have a highly conserved evolutionary pattern. Polyploidy is the primary reason for the expansion of the ARF family after quinoa domestication. The expression patterns of CqARFs in different tissues have been differentiated, and CqARF2, 5, 9 and 10 from class A have the characteristics of local heterogeneous expression in different regions of roots, which may be the key factors for crops to respond in complex environments. Overall, we examined the evolution and expansion of ARFs in representative domesticated crops using the genome, transcriptome, and molecular biology and discovered a class A ARF-centered heterogeneous expression network that played an important role in auxin signaling and environmental responses. We provide new insights into how ARFs promote domesticated crop adaptation to artificial selection by polyploid expansion.

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Data Availability

All sequence data used in this paper are already publicly available. The datasets supporting the conclusions of this article are included within the article and its Additional files.

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Acknowledgements

We thank all the colleagues in our laboratory for providing useful discussions and technical assistance.

Funding

This research was supported by a Study on Entrepreneurship Training Program for College Students (202010626015) and Function Study of FtbHLH Transcription Factor Regulating Tartary Buckwheat Fruit Dehiscence (2021YFH0086) of Sichuan Province Science and Technology Support Program. Funds were used for the design of the study, collection, analysis, and interpretation of data, and in writing the manuscript, as well as in the open access payment.

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  1. Wenjun Sun and Haomiao Yu contributed equally to this work.

Authors and Affiliations

  1. College of Life Science, Sichuan Agricultural University, Ya’an, 625014, China

    Wenjun Sun, Haomiao Yu, Yuan Yuan, Sijiao Wang & Hui Chen

  2. State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Key Laboratory of Major Crop Diseases and Rice Research Institute, Sichuan Agricultural University, Chengdu, 611130, China

    Zhaotang Ma

  3. Key Laboratory of Coarse Cereal Processing, Ministry of Agriculture Rural Affairs, School of Pharmacy and Bioengineering, Chengdu University, Chengdu, 610106, China

    Jun Yan & Xinran Xu

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  1. Wenjun Sun
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Contributions

W-JS and H-C planned and designed the research. H-MY and W-JS analyzed data. H-MY wrote the original manuscript. W-JS and Z-TM identified ARF family of quinoa and visualized structures of CqARFs. W-JS and X-RX determined the ARFs duplication types of quinoa and Arabidopsis. Y-Y and S-JW performed CqARF genes chromosome distribution, gene duplication, and synteny analysis. H-MY and W-JS detected CqARFs expression levels by qRT-PCR and the correlation of gene expression was analyzed. All authors read and approved the final manuscript.

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Correspondence to Hui Chen.

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Sun, W., Yu, H., Ma, Z. et al. Molecular Evolution and Local Root Heterogeneous Expression of the Chenopodium quinoa ARF Genes Provide Insights into the Adaptive Domestication of Crops in Complex Environments. J Mol Evol 89, 287–301 (2021). https://doi.org/10.1007/s00239-021-10005-5

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