Overexpression of tonoplast Ca2+‐ATPase in guard cells synergistically enhances stomatal opening and drought tolerance

• Published in: Journal of integrative plant biology 2024-08, Vol.66 (8), p.1587-1602
• Main Authors: Su, Jinghan, He, Bingqing, Li, Peiyuan, Yu, Baiyang, Cen, Qiwen, Xia, Lingfeng, Jing, Yi, Wu, Feibo, Karnik, Rucha, Xue, Dawei, Blatt, Michael R., Wang, Yizhou
• Format: Article
• Language: English
• Subjects: Abscisic acid; ACA11; Adenosine triphosphatase; Calcium; Calcium ions; drought; Drought resistance; Guard cells; modeling; Plant cells; Plant growth; Stomata; Transgenic plants; Water loss
• ISSN: 1672-9072; 1744-7909; 1744-7909
• DOI: 10.1111/jipb.13721

ABSTRACT Stomata play a crucial role in plants by controlling water status and responding to drought stress. However, simultaneously improving stomatal opening and drought tolerance has proven to be a significant challenge. To address this issue, we employed the OnGuard quantitative model, which accurately represents the mechanics and coordination of ion transporters in guard cells. With the guidance of OnGuard, we successfully engineered plants that overexpressed the main tonoplast Ca2+‐ATPase gene, ACA11, which promotes stomatal opening and enhances plant growth. Surprisingly, these transgenic plants also exhibited improved drought tolerance due to reduced water loss through their stomata. Again, OnGuard assisted us in understanding the mechanism behind the unexpected stomatal behaviors observed in the ACA11 overexpressing plants. Our study revealed that the overexpression of ACA11 facilitated the accumulation of Ca2+ in the vacuole, thereby influencing Ca2+ storage and leading to an enhanced Ca2+ elevation in response to abscisic acid. This regulatory cascade finely tunes stomatal responses, ultimately leading to enhanced drought tolerance. Our findings underscore the importance of tonoplast Ca2+‐ATPase in manipulating stomatal behavior and improving drought tolerance. Furthermore, these results highlight the diverse functions of tonoplast‐localized ACA11 in response to different conditions, emphasizing its potential for future applications in plant enhancement. Overexpression of the tonoplast Ca2+‐ATPase gene ACA11 increases Ca2+ accumulation in the vacuole, promoting stomatal opening, carbon assimilation, and plant growth under optimal conditions. However, during drought, the over‐accumulation of vacuolar Ca2+ triggers a larger release of cytosolic Ca2+, resulting in stomatal closure and enhancing drought tolerance.