Gene duplication and evolution dynamics in the homeologous regions harboring multiple prolamin and resistance gene families in hexaploid wheat

Authors: HUO, NAXIN - University Of California, Davis; ZHANG, SHENGLI - Henan Institute Of Science And Technology; ZHU, TINGTING - University Of California, Davis; DONG, LINGLI - Chinese Academy Of Sciences; WANG, YI - University Of California, Davis; Mohr, Toni; HU, TIEZHU - Henan Institute Of Science And Technology; LIU, ZHIYONG - Chinese Academy Of Sciences; DVORAK, JAN - University Of California, Davis; LUO, MING-CHENG - University Of California, Davis; WANG, DAOWEN - Chinese Academy Of Sciences; LEE, JONG-YEOL - National Institute For Agricultural Science & Technology; Altenbach, Susan; Gu, Yong

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/3/2018
Publication Date: 5/23/2018
Citation: Huo, N., Zhang, S., Zhu, T., Dong, L., Wang, Y., Mohr, T.J., Hu, T., Liu, Z., Dvorak, J., Luo, M., Wang, D., Lee, J., Altenbach, S.B., Gu, Y.Q. 2018. Gene duplication and evolution dynamics in the homeologous regions harboring multiple prolamin and resistance gene families in hexaploid wheat. Frontiers in Plant Science. 9:673. https://doi.org/10.3389/fpls.2018.00673.
DOI: https://doi.org/10.3389/fpls.2018.00673

Interpretive Summary: The content of prolamins, the major seed storage proteins of wheat, and disease resistance are two important traits in wheat breeding and production. However, wheat is a polyploid species containing three related A, B, and D subgenomes, making genetic studies on these traits more complicated. In this study, we sequenced, analyzed, and compared genomic regions harboring interleaved prolamin and disease resistance genes to better understand their structure, evolution, and functions in different wheat genomes. Our results indicated that both prolamin and resistance genes have experienced fast and independent changes in the A, B, and D genomes. The rapid evolution provides insights into the large differences in the end-use quality and disease resistance traits observed in different wheat cultivars. A complete set of prolamin gene sequences was identified through the data analysis, and the expression levels of the genes were measured using next-generation sequencing technology. We found that the A genome contributes the least to prolamin expression while the B and D genomes contribute more and at similar levels. The knowledge gained in this study will be useful for developing breeder selection strategies to improve the grain quality and resistance traits of wheat.

Technical Abstract: Prolamin-associated end-use quality and disease resistance are important traits in wheat breeding and production. The genetic loci controlling these traits are highly complex because of the large number of their gene family members present in all three homeologous A, B and D genomes in hexaploid bread wheat. In this study, orthologous regions harboring multiple prolamin and resistance gene loci were examined to understand gene duplication and evolution in different wheat genomes, including the progenitor D genome from Ae. tauschii. Comparison of the two orthologous D regions from the hexaploid wheat Chinese Spring and diploid Ae. tauschii indicated that these closely related genomes were considerably different due to the presence or absence of multiple large structure variations (over 100 kb). Overall 44% of the Ae. tauschii and 71% of the Chinese Spring sequence (including 79 total genes) are not shared. We found that gene rearrangement events, including differential duplication and deletion in the A, B and D regions, complicated colinearity analysis of prolamin and resistance gene family members, suggesting rapid evolution of these two gene families after the separation of the three wheat genomes. We hypothesize that this fast evolution can be attributed to the co-evolution of the two gene families that are interleaved within a high recombination region. The identification of a full set of prolamin genes facilitated transcriptome profiling and revealed that the A genome contributes the least to prolamin expression because of its smaller number of expressed intact genes and their low expression levels, while the B and D genomes contribute more and at similar levels. These results have implications for breeder decisions in simultaneously selecting for disease resistance and wheat end-use properties.