Null mutants of a tomato Rho of plants exhibit enhanced water use efficiency without a penalty to yield

Author:

Puli Mallikarjuna R.1ORCID,Muchoki Purity1ORCID,Yaaran Adi1ORCID,Gershon Noga1ORCID,Dalal Ahan1ORCID,Nalufunjo Felista1ORCID,Dagan Yoav1ORCID,Rosental Leah2ORCID,Abadi Shiran1ORCID,Haber Zachary1ORCID,Silva Lucas3ORCID,Brotman Yariv2,Sade Nir1ORCID,Yalovsky Shaul1ORCID

Affiliation:

1. School of Plant Sciences and Food Security, Tel Aviv University, Tel Aviv 6997801, Israel

2. Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 8410501, Israel

3. Environmental Studies and Biology, University of Oregon, Eugene, OR 97403

Abstract

Improving water use efficiency in crops is a significant challenge as it involves balancing water transpiration and CO 2 uptake through stomatal pores. This study investigates the role of SlROP9, a tomato Rho of Plants protein, in guard cells and its impact on plant transpiration. The results reveal that SlROP9 null mutants exhibit reduced stomatal conductance while photosynthetic CO 2 assimilation remains largely unaffected. Notably, there is a notable decrease in whole-plant transpiration in the rop9 mutants compared to the wild type, especially during noon hours when the water pressure deficit is high. The elevated stomatal closure observed in rop9 mutants is linked to an increase in reactive oxygen species formation. This is very likely dependent on the respiratory burst oxidase homolog (RBOH) NADPH oxidase and is not influenced by abscisic acid (ABA). Consistently, activated ROP9 can interact with RBOHB in both yeast and plants. In diverse tomato accessions, drought stress represses ROP9 expression, and in Arabidopsis stomatal guard cells, ABA suppresses ROP signaling. Therefore, the phenotype of the rop9 mutants may arise from a disruption in ROP9-regulated RBOH activity. Remarkably, large-scale field experiments demonstrate that the rop9 mutants display improved water use efficiency without compromising fruit yield. These findings provide insights into the role of ROPs in guard cells and their potential as targets for enhancing water use efficiency in crops.

Funder

Israel Science Foundation

United States - Israel Binational Agricultural Research and Development Fund

Israel Innovation Authority

Publisher

Proceedings of the National Academy of Sciences

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