Cytokinin and MAX2 signaling pathways act antagonistically in drought adaptation of Arabidopsis thaliana
Kien Huu Nguyen,
Zihan Li,
Chengliang Wang,
Chien Van Ha,
Cuong Duy Tran,
Mostafa Abdelrahman,
Xuan Hoi Pham,
Khuat Huu Trung,
Tran Dang Khanh,
Ha Duc Chu,
Mohammad Golam Mostofa,
Yasuko Watanabe,
Yaping Wang,
Yuchen Miao,
Keiichi Mochida,
Sikander Pal,
Weiqiang Li,
Lam-Son Phan Tran
Affiliations
Kien Huu Nguyen
Agricultural Genetics Institute, Vietnam Academy of Agricultural Sciences, Pham Van Dong Str., Hanoi, 100000, Viet Nam
Zihan Li
Jilin Da'an Agro-ecosystem National Observation Research Station, Changchun Jingyuetan Remote Sensing Experiment Station, State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China
Chengliang Wang
Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, School of Life Sciences, Anhui Normal University, Wuhu, 241000, China
Chien Van Ha
Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, TX 79409, USA
Cuong Duy Tran
Agricultural Genetics Institute, Vietnam Academy of Agricultural Sciences, Pham Van Dong Str., Hanoi, 100000, 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
Xuan Hoi Pham
Agricultural Genetics Institute, Vietnam Academy of Agricultural Sciences, Pham Van Dong Str., Hanoi, 100000, Viet Nam
Khuat Huu Trung
Agricultural Genetics Institute, Vietnam Academy of Agricultural Sciences, Pham Van Dong Str., Hanoi, 100000, Viet Nam
Tran Dang Khanh
Agricultural Genetics Institute, Vietnam Academy of Agricultural Sciences, Pham Van Dong Str., Hanoi, 100000, Viet Nam; Jilin Da'an Agro-ecosystem National Observation Research Station, Changchun Jingyuetan Remote Sensing Experiment Station, State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China; Anhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, School of Life Sciences, Anhui Normal University, Wuhu, 241000, China; Institute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, TX 79409, USA; Faculty of Agricultural Technology, University of Engineering and Technology, Vietnam National University Hanoi, Xuan Thuy Road, Cau Giay District, Hanoi City 122300, Viet Nam; Department of Energy Plant Research Laboratory, Michigan State University, East Lansing 48824, Michigan, USA; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, 48824, Michigan, USA; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, 230-0045, Japan; State Key Laboratory of Cotton Biology, Henan Joint International Laboratory for Crop Multi-Omics Research, School of Life Sciences, Henan University, No. 85 Jinming Road, Kaifeng, 475004, China; 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; Crop Physiology Laboratory, Department of Botany University of Jammu, Jammu 180006, India; Vietnam National University of Agriculture, Hanoi City 131000, Vietnam
Ha Duc Chu
Faculty of Agricultural Technology, University of Engineering and Technology, Vietnam National University Hanoi, Xuan Thuy Road, Cau Giay District, Hanoi City 122300, Viet Nam
Mohammad Golam Mostofa
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing 48824, Michigan, USA; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, 48824, Michigan, USA
Yasuko Watanabe
RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, 230-0045, Japan
Yaping Wang
State Key Laboratory of Cotton Biology, Henan Joint International Laboratory for Crop Multi-Omics Research, School of Life Sciences, Henan University, No. 85 Jinming Road, Kaifeng, 475004, China
Yuchen Miao
State Key Laboratory of Cotton Biology, Henan Joint International Laboratory for Crop Multi-Omics Research, School of Life Sciences, Henan University, No. 85 Jinming Road, Kaifeng, 475004, China
Keiichi Mochida
RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, 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
Sikander Pal
Crop Physiology Laboratory, Department of Botany University of Jammu, Jammu 180006, India
Weiqiang Li
Jilin Da'an Agro-ecosystem National Observation Research Station, Changchun Jingyuetan Remote Sensing Experiment Station, State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China; State Key Laboratory of Cotton Biology, Henan Joint International Laboratory for Crop Multi-Omics Research, School of Life Sciences, Henan University, No. 85 Jinming Road, Kaifeng, 475004, China; Corresponding authors.
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.
Understanding the mechanisms, especially those associated with phytohormones, of plant drought adaptation is crucial for sustaining agricultural production in the era of climate change. Arabidopsis histidine kinases (AHKs), an integral part of the cytokinin signaling pathway, and more axillary growth 2 (MAX2), a key component of the strigolactone and karrikin signaling pathways are reported to act as negative and positive regulators, respectively, in plant adaption to drought. However, the potential interaction between these singaling pathways in plant drought adaptation is not fully understood. To address this query, we assessed drought tolerance levels and associated phenotypic and physiological traits of the max2 single mutant, ahk2 ahk3 double mutant, ahk2 ahk3 max2 triple mutant, and wild-type (WT) Arabidopsis thaliana plants. Our findings revealed a distinct hierarchy in drought tolerance among these genotypes, as indicated by the differences in plant growth and stress survival rates. Specifically, the max2 mutant displayed the lowest drought tolerance level, followed by WT, ahk2 ahk3 max2, and ahk2 ahk3 plants. Additionally, the observed changes in leaf relative water content, leaf surface temperature, and cuticle formation were coherently aligned with the observed hierarchy of drought tolerance levels. Under drought conditions, the max2 mutant exhibited higher oxidative stress and membrane damage, as evidenced by increased levels of reactive oxygen species (ROS), malondialdehyde, and electrolyte leakage. In contrast, the ahk2 ahk3 and ahk2 ahk3 max2 mutants showed low and intermediate levels, respectively, for these parameters. The max2 mutant displayed reduced sensitivity, whereas ahk2 ahk3 and ahk2 ahk3 max2 mutants demonstrated high and intermediate sensitivities, respectively, to exogenous abscisic acid (ABA) treatments. Additionally, the expression analysis of several genes associated with the investigated drought tolerance-related traits showed a positive correlation between the transcript levels and corresponding trait(s) in both mutant and WT plants under drought conditions. Our results collectively indicate the presence of an antagonistic interaction between AHK and MAX2 signaling pathways in plant drought adaptation, impacting ABA responsiveness, leaf water retention, cuticle development, and ROS homestasis. The findings of this study provide a valuable foundation for developing agricultural methods to improve plant drought resilience.
