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New insights into the evolution and expression dynamics of invertase gene family in Solanum lycopersicum

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Abstract

Invertases catalyze the irreversible hydrolysis of sucrose into glucose and fructose and thus play key roles in carbon metabolism and plant development. To gain insights into their evolutional and functional relationships, we conducted genome-wide analyses of invertase genes in tomato and other species, focusing on their evolution and expression dynamics. The analyses unexpectedly identified in the tomato genome 5 pseudo invertsase sequences and 5 non-functional cell wall invertases (CWINs) lacking the critical β-fructosidase motif or other amino acids required for hydrolyzing sucrose. Based on their phylogeny relationship and exon–intron structure, we speculated that the invertase gene family could arose from different ancestral genes. The acid invertase gene family, comprised of CWIN and vacuolar invertase (VIN), expanded through segmental and tandem duplication. Analysis of functional divergence suggests site-specific shifted evolutionary rate (Type-I) have played an important role in evolutionary novelties after acid invertase gene duplication in plants. Finally, paralogs within each of the CWIN, VIN and CIN subfamilies exhibited diverse expression responses to the same set of stress treatments including salt and temperature stresses, probably reflecting functional adaptability of the invertase genes during evolution.

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Acknowledgements

The authors would like to thank Prof. Yong-Ling Ruan for conceptualizing preliminarily the experiments.

Funding

This research was partially supported by National Key Research and Development Program of China (2017YFD0101902), State Key Laboratory Breeding Base for the Zhejiang Sustainable Pest and Disease Control (2010DS700124-ZZ1903 and 2010DS700124-ZZ1807), National Natural Science Foundation of China (31772294), National Key Research and Development Program (2018YCGC005), Zhejiang Provincial Major Agricultural Science and Technology Projects of New Varieties Breeding (2016C02051), Zhejiang Provincial Natural Science Foundation of China (LY18C150008), General Program from the National key research and development program (2018YFD1000800), The earmarked fund for China Agriculture Research System (CARS-23-G-44).

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  1. Huawei Wei and Songlin Chai have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China

    Huawei Wei, Songlin Chai, Yuan Cheng, Meiying Ruan, Qingjing Ye, Rongqing Wang, Zhuping Yao, Guozhi Zhou & Hongjian Wan

  2. College of Horticulture, Anhui Agricultural University, Hefei, 230036, China

    Huawei Wei & Yougen Chen

  3. College of Horticulture and Gardening, Yangtze University, Jingzhou, 434025, China

    Songlin Chai & Luzhao Pan

  4. Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, College of Agriculture and Food Science, Zhejiang A & F University, Lin’an, 311300, Zhejiang, China

    Lei Ru

  5. China-Australia Research Centre for Crop Improvement, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China

    Hongjian Wan

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  1. Huawei Wei
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Contributions

H.W. and S.C. conceived and designed the research. L.R., L.P., Y.C, M.R., Q.Y., performed the experiments. Z.Y., G.Z., R.W., Y.C. and H.W. analyzed the data and wrote the paper. H.W. revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Hongjian Wan.

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Wei, H., Chai, S., Ru, L. et al. New insights into the evolution and expression dynamics of invertase gene family in Solanum lycopersicum. Plant Growth Regul 92, 205–217 (2020). https://doi.org/10.1007/s10725-020-00631-2

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