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Evolution of cytosolic and organellar invertases empowered the colonization and thriving of land plants

文献类型： 外文期刊

作者： Wan, Hongjian 1 ; Zhang, Youjun 2 ; Wu, Limin 4 ; Zhou, Guozhi 1 ; Pan, Luzhao 1 ; Fernie, Alisdair R. 2 ; Ruan, Yong-Ling 5 ;

作者机构： 1.Zhejiang Acad Agr Sci, Inst Vegetables, State Key Lab Managing Biot & Chem Threats Qual &, Hangzhou 310021, Peoples R China

2.Ctr Plant Syst Biol & Biotechnol, Plovdiv 4000, Bulgaria

3.Max Planck Inst Mol Plant Physiol, Dept Mol Physiol, D-14476 Potsdam, Germany

4.CSIRO, Food & Agr, Canberra, ACT 2601, Australia

5.Northwest A&F Univ, State Key Lab Crop Stress Biol Arid Areas, Xianyang 712100, Peoples R China

6.Northwest A&F Univ, Coll Hort, Xianyang 712100, Peoples R China

7.Australian Natl Univ, Res Sch Biol, Div Plant Sci, Canberra, ACT 2601, Australia

期刊名称：PLANT PHYSIOLOGY （ 影响因子：7.4； 五年影响因子：8.7 ）

ISSN： 0032-0889

年卷期： 2023 年

页码：

收录情况： SCI

摘要： The molecular innovation underpinning efficient carbon and energy metabolism during evolution of land plants remains largely unknown. Invertase-mediated sucrose cleavage into hexoses is central to fuel growth. Why some cytoplasmic invertases (CINs) function in the cytosol, whereas others operate in chloroplasts and mitochondria, is puzzling. We attempted to shed light on this question from an evolutionary perspective. Our analyses indicated that plant CINs originated from a putatively orthologous ancestral gene in cyanobacteria and formed the plastidic CIN (& alpha;1 clade) through endosymbiotic gene transfer, while its duplication in algae with a loss of its signal peptide produced the & beta; clade CINs in the cytosol. The mitochondrial CINs (& alpha;2) were derived from duplication of the plastidic CINs and coevolved with vascular plants. Importantly, the copy number of mitochondrial and plastidic CINs increased upon the emergence of seed plants, corresponding with the rise of respiratory, photosynthetic, and growth rates. The cytosolic CIN (& beta; subfamily) kept expanding from algae to gymnosperm, indicating its role in supporting the increase in carbon use efficiency during evolution. Affinity purification mass spectrometry identified a cohort of proteins interacting with & alpha;1 and 2 CINs, which points to their roles in plastid and mitochondrial glycolysis, oxidative stress tolerance, and the maintenance of subcellular sugar homeostasis. Collectively, the findings indicate evolutionary roles of & alpha;1 and & alpha;2 CINs in chloroplasts and mitochondria for achieving high photosynthetic and respiratory rates, respectively, which, together with the expanding of cytosolic CINs, likely underpin the colonization of land plants through fueling rapid growth and biomass production. The diversification and expansion of cytosolic and organellar invertases represent a key molecular innovation underpinning efficient carbon and energy metabolism for the evolution of land plants.

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