Leaf Gas Film 1 promotes glycerol ester accumulation and formation of a tight root barrier to radial O2 loss in rice

Author:

Jiménez Juan de la Cruz12ORCID,Noorrohmah Siti23ORCID,Suresh Kiran4ORCID,Zeisler-Diehl Viktoria V4ORCID,Peralta Ogorek Lucas León15ORCID,Herzog Max1ORCID,Pellegrini Elisa1ORCID,Nagai Keisuke6ORCID,Ashikari Motoyuki6,Takahashi Hirokazu2ORCID,Pedersen Ole17ORCID,Schreiber Lukas4ORCID,Nakazono Mikio28ORCID

Affiliation:

1. Department of Biology, University of Copenhagen , Universitetsparken 4, 3rd floor, Copenhagen 2100 , Denmark

2. Graduate School of Bioagricultural Sciences, Nagoya University , Furo-cho, Chikusa, Nagoya 464-8601 , Japan

3. Research Center for Applied Botany, Research Organization for Life Sciences and Environment, National Research and Innovation Agency , Jl. Raya Bogor KM.46, Cibinong, Bogor, West Java 16911 , Indonesia

4. Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn , Kirschallee 1, Bonn, 53115 , Germany

5. School of Biosciences, University of Nottingham , Sutton Bonington LE12 5RD , UK

6. Bioscience and Biotechnology Center of Nagoya University , Furo-Cho, Chikusa, Nagoya, Aichi 464-8602 , Japan

7. School of Biological Sciences, The University of Western Australia , 35 Stirling Highway, Crawley, WA 6009 , Australia

8. School of Agriculture and Environment, The University of Western Australia , 35 Stirling Highway, Crawley, WA 6009 , Australia

Abstract

Abstract Rice (Oryza sativa L.) and many other wetland plants form an apoplastic barrier in the outer parts of the roots to restrict radial O2 loss to the rhizosphere during soil flooding. This barrier facilitates longitudinal internal O2 diffusion via gas-filled tissues from shoot to root apices, enabling root growth in anoxic soils. We tested the hypothesis that Leaf Gas Film 1 (LGF1), which influences leaf hydrophobicity in rice, plays a crucial role in tight outer apoplastic barrier formation in rice roots. We examined the roots of a rice mutant (dripping wet leaf 7, drp7) lacking functional LGF1, its wild type, and an LGF1 overexpression line for their capacity to develop outer apoplastic barriers that restrict radial O2 loss. We quantified the chemical composition of the outer part of the root and measured radial O2 diffusion from intact roots. The drp7 mutant exhibited a weak barrier to radial O2 loss compared to the wild type. However, introducing functional LGF1 into the mutant fully restored tight barrier function. The formation of a tight barrier to radial O2 loss was associated with increased glycerol ester levels in exodermal cells, rather than differences in total root suberization or lignification. These results demonstrate that, in addition to its role in leaf hydrophobicity regulation, LGF1 plays an important role in controlling the function of the outer apoplastic barriers in roots. Our study suggests that increased deposition of glycerol esters in the suberized root exodermis establishes a tight barrier to radial O2 loss in rice roots.

Funder

The European Union under a Marie Skłodowska-Curie Postdoctoral Fellowship

Japanese Society for Science Promotion

The Independent Research Fund Denmark

Danish International Development Agency

German Research Foundation

Grant-in-Aid for Transformative Research Areas

Publisher

Oxford University Press (OUP)

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