The vacuolar H+/Ca transporter CAX1 participates in submergence and anoxia stress responses

Authors: YANG, JIAN - CHILDREN'S NUTRITION RESEARCH CENTER (CNRC); MATHEW, INY ELIZABETH - CHILDREN'S NUTRITION RESEARCH CENTER (CNRC); RHEIN, HORMAT - CHILDREN'S NUTRITION RESEARCH CENTER (CNRC); BARKER, RICHARD - UNIVERSITY OF WISCONSIN; GUO, QI - SOUTHERN CROSS UNIVERSITY; BRUNELLO, LUCA - INSTITUTE OF LIFE SCIENCE, SCUOLA SUPERIORE SANT'ANNA; LORETI, ELENA - NATIONAL RESEARCH COUNCIL - ITALY; BARKLA, BRONWYN - SOUTHERN CROSS UNIVERSITY; GILROY, SIMON - UNIVERSITY OF WISCONSIN; PERATA, PIERDOMENICO - INSTITUTE OF LIFE SCIENCE, SCUOLA SUPERIORE SANT'ANNA; HIRSCHI, KENDAL - CHILDREN'S NUTRITION RESEARCH CENTER (CNRC)

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/17/2022
Publication Date: 8/16/2022
Citation: Yang, J., Mathew, I., Rhein, H., Barker, R., Guo, Q., Brunello, L., Loreti, E., Barkla, B., Gilroy, S., Perata, P., Hirschi, K.D. 2022. The vacuolar H+/Ca transporter CAX1 participates in submergence and anoxia stress responses. Plant Physiology. 190(4):2617-2636. https://doi.org/10.1093/plphys/kiac375.
DOI: https://doi.org/10.1093/plphys/kiac375

Interpretive Summary: Plants are frequently exposed to low oxygen conditions, especially during flooding. Flooding of crops is a substantial economic hardship for agricultural production and there is a critical need to engineer crops that can tolerate submergence for extended periods. This work demonstrates that plants that cannot move calcium into storage compartments due to a genetic mutation can accept limited oxygen conditions and submergence. This is surprising because the removal of a gene causes an improvement in the plant during flooding conditions. This work may allow the development of improved crops if we can disrupt this calcium storage mechanism during flooding conditions.

Technical Abstract: A plant's oxygen supply can vary from normal (normoxia) to total depletion (anoxia). Tolerance to anoxia is relevant to wetland species, rice (Oryza sativa) cultivation, and submergence tolerance of crops. Decoding and transmitting calcium (Ca) signals may be an important component to anoxia tolerance; however, the contribution of intracellular Ca transporters to this process is poorly understood. Four functional cation/proton exchangers (CAX1–4) in Arabidopsis (Arabidopsis thaliana) help regulate Ca homeostasis around the vacuole. Our results demonstrate that cax1 mutants are more tolerant to both anoxic conditions and submergence. Using phenotypic measurements, RNA-sequencing, and proteomic approaches, we identified cax1-mediated anoxia changes that phenocopy changes present in anoxia-tolerant crops: altered metabolic processes, diminished reactive oxygen species production post anoxia, and altered hormone signaling. Comparing wild-type and cax1 expressing genetically encoded Ca indicators demonstrated altered cytosolic Ca signals in cax1 during reoxygenation. Anoxia-induced Ca signals around the plant vacuole are involved in the control of numerous signaling events related to adaptation to low oxygen stress. This work suggests that cax1 anoxia response pathway could be engineered to circumvent the adverse effects of flooding that impair production agriculture.