Comparative transcriptome analysis of respiration-related genes in nodules of phosphate-deficient soybean (Glycine max cv. Williams 82)
Saad Sulieman,
Chien Van Ha,
Dung Tien Le,
Mostafa Abdelrahman,
Cuong Duy Tran,
Yasuko Watanabe,
Maho Tanaka,
Zaid Ulhassan,
Mohamed S. Sheteiwy,
Sunil S. Gangurde,
Keiichi Mochida,
Motoaki Seki,
Lam-Son Phan Tran
Affiliations
Saad Sulieman
Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North 13314, Sudan; Corresponding authors.
Chien Van Ha
Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, TX 79409, USA
Dung Tien Le
VKTECH Research Center, NTT Hi-Tech Institute, Nguyen Tat Thanh University, 298A-300A Nguyen Tat Thanh Street, District 4, Ho Chi Minh City, 70000, Viet Nam
Mostafa Abdelrahman
Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, TX 79409, USA
Cuong Duy Tran
Genetic Engineering Department, Agricultural Genetics Institute, Vietnamese Academy of Agricultural Science, Pham Van Dong Street, Hanoi 100000, Viet Nam
Yasuko Watanabe
Bioproductivity Informatics Research Team, RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Japan
Maho Tanaka
Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan; Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
Zaid Ulhassan
Institute of Crop Science, Ministry of Agriculture and Rural Affairs Key Laboratory of Spectroscopy Sensing, Zhejiang University, Hangzhou 310058, China
Mohamed S. Sheteiwy
Department of Integrative Agriculture, College of Agriculture and Veterinary Medicine, United Arab Emirates University, P.O. Box 15551, Al Ain, Abu Dhabi, UAE; Department of Agronomy, Faculty of Agriculture, Mansoura University, Mansoura 35516, Egypt
Sunil S. Gangurde
International Crops Research Institute for the Semi-Arid Tropics, Hyderabad 502324, India
Keiichi Mochida
Bioproductivity Informatics Research Team, RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Japan; School of Information and Data Sciences, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, Japan; Kihara Institute for Biological Research, Yokohama City University, 641-12 Maioka-cho, Totsuka-ku, Yokohama, Kanagawa 244-0813, Japan; RIKEN Baton Zone Program, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama 230-0045, Japan
Motoaki Seki
Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan; Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan; Kihara Institute for Biological Research, Yokohama City University, 641-12 Maioka-cho, Totsuka-ku, Yokohama, Kanagawa 244-0813, Japan
Lam-Son Phan Tran
Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, TX 79409, USA; Corresponding authors.
A transcriptome analysis was used to compare the nodule transcriptomes of the model soybean ‘Williams 82’ inoculated with two Bradyrhizobium diazoefficiens strains (USDA110 vs. CB1809) under phosphate (Pi) deficiency. The entire dataset revealed a core set of low-Pi-responsive genes and recognized enormous differential transcriptional changes between the Pi-deprived USDA110-nodules and CB1809-nodules. The lower symbiotic efficiency of the Pi-starved USDA110 nodules was ascribed to the downregulation of an F1-ATPase gene engaged in oxidative phosphorylation, more likely contributing to diminished ATP production. To cope with energy shortage caused by Pi stress, the Pi-deprived USDA110-nodules preferentially upregulated the expression of a large number of genes encoding enzymes implicated in specialized energy-demanding pathways, such as the mitochondrial respiratory chain (i.e., cytochrome c oxidase), alcoholic fermentation (i.e., pyruvate decarboxylase and alcohol dehydrogenase) and glycolysis (e.g., hexokinase, phosphofructokinase, glyceraldehyde‐3‐phosphate dehydrogenase and pyruvate kinase). These respiratory adjustments were likely associated with higher metabolic cost and redox imbalance, thereby, negatively affecting nodule symbiosis under Pi deprivation. In contrast, the Pi-starved CB1809-nodules reduced the metabolic cost by regulating a lower number of genes and increasing the expression of genes encoding proteins implicated in non-phosphorylating bypasses (e.g., flavoprotein alpha and flavoprotein:ubiqionone oxidoreductase), which could promote the carbohydrate utilization efficiency and energy metabolism. Notably, the upregulation of a transcript encoding a malate dehydrogenase could boost the CB1809-nodules under Pi stress. The dynamic shifts in energy metabolism in the Pi-deprived USDA110-nodules and CB1809-nodules could be transformative to upgrade the mechanistic/conceptual understandings of soybean adaptation to Pi deficiency at the transcriptional level.
