Evolutionary expansion and functional divergence of sugar transporters in Saccharum (S. spontaneum and S. officinarum). (8th December 2020)

• Record Type: Journal Article
• Authors: Zhang, Qing; Hua, Xiuting; Liu, Hong; Yuan, Yuan; Shi, Yan; Wang, Zhengchao; Zhang, Muqing; Ming, Ray; Zhang, Jisen
• Is Part Of: Plant journal. Volume 105:Number 4(2021)
• Page Start: 884
• Page End: 906
• Publication Date: 2020-12-08
• Subjects: sugar transporter -- evolutionary expansion -- functional divergence -- Saccharum spontaneum -- Saccharum officinarum; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15076
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: The sugar transporter ( ST ) family is considered to be the most important gene family for sugar accumulation, but limited information about the ST family in the important sugar‐yielding crop Saccharum is available due to its complex genetic background. Here, 105 ST genes were identified and clustered into eight subfamilies in Saccharum spontaneum . Comparative genomics revealed that tandem duplication events contributed to ST gene expansions of two subfamilies, PLT and STP, in S. spontaneum, indicating an early evolutionary step towards high sugar content in Saccharum . The analyses of expression patterns were based on four large datasets with a total of 226 RNA sequencing samples from S. spontaneum and Saccharum officinarum . The results clearly demonstrated 50 ST genes had different spatiotemporal expression patterns in leaf tissues, 10 STs were specifically expressed in the stem, and 10 STs responded to the diurnal rhythm. Heterologous expression experiments in the defective yeast strain EBY.VW4000 indicated STP13, pGlcT2, VGT3, and TMT4 are the STs with most affinity for glucose/fructose and SUT1_T1 has the highest affinity to sucrose. Furthermore, metabolomics analysis suggested STP7 is a sugar starvation‐induced gene and STP13 has a function in retrieving sugar in senescent tissues. PLT11, PLT11_T1, TMT3, and TMT4 contributed to breaking the limitations of the storage sink. SUT1, SUT1_T1, PLT11, TMT4, pGlcT2, and VGT3 responded for different functions in these two Saccharum species. This study demonstrated the evolutionary expansion and functional divergence of the ST gene family and will enable the further investigation of the molecular mechanism of sugar metabolism in Saccharum . Significance Statement: An early evolutionary step towards high sugar content in Saccharum was indicated to be caused by recent tandem duplication events in Saccharum spontaneum, and functional divergence of the ST family between S. spontaneum and Saccharum officinarum was further unveiled based on heterologous expression experiments, a large set of transcriptome data, and metabolomics analysis. This study will enable the further investigation of the molecular mechanism of sugar metabolism in Saccharum .