Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells

Juntaro Negi, Shintaro Munemasa, Boseok Song, Ryosuke Tadakuma, Mayumi Fujita, Tamar Azoulay-Shemer, Cawas B. Engineer, Kensuke Kusumi, Ikuo Nishida, Julian I. Schroeder, Koh Iba

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Stomatal guard cells develop unique chloroplasts in land plant species. However, the developmental mechanisms and function of chloroplasts in guard cells remain unclear. In seed plants, chloroplast membrane lipids are synthesized via two pathways: the prokaryotic and eukaryotic pathways. Here we report the central contribution of endoplasmic reticulum (ER)-derived chloroplast lipids, which are synthesized through the eukaryotic lipid metabolic pathway, in the development of functional guard cell chloroplasts. We gained insight into this pathway by isolating and examining an Arabidopsis mutant, gles1 (green less stomata 1), which had achlorophyllous stomatal guard cells and impaired stomatal responses to CO2 and light. The GLES1 gene encodes a small glycine-rich protein, which is a putative regulatory component of the trigalactosyldiacylglycerol (TGD) protein complex that mediates ER-to-chloroplast lipid transport via the eukaryotic pathway. Lipidomic analysis revealed that in the wild type, the prokaryotic pathway is dysfunctional, specifically in guard cells, whereas in gles1 guard cells, the eukaryotic pathway is also abrogated. CO2-induced stomatal closing and activation of guard cell S-type anion channels that drive stomatal closure were disrupted in gles1 guard cells. In conclusion, the eukaryotic lipid pathway plays an essential role in the development of a sensing/ signaling machinery for CO2 and light in guard cell chloroplasts.

Original languageEnglish
Pages (from-to)9038-9043
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number36
DOIs
Publication statusPublished - Sep 4 2018

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Chloroplasts
Metabolic Networks and Pathways
Arabidopsis
Lipids
Light
Endoplasmic Reticulum
Embryophyta
Eukaryotic Cells
Membrane Lipids
Glycine
Anions
Seeds
Proteins
Genes

All Science Journal Classification (ASJC) codes

  • General

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Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells. / Negi, Juntaro; Munemasa, Shintaro; Song, Boseok; Tadakuma, Ryosuke; Fujita, Mayumi; Azoulay-Shemer, Tamar; Engineer, Cawas B.; Kusumi, Kensuke; Nishida, Ikuo; Schroeder, Julian I.; Iba, Koh.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 36, 04.09.2018, p. 9038-9043.

Research output: Contribution to journalArticle

Negi, Juntaro ; Munemasa, Shintaro ; Song, Boseok ; Tadakuma, Ryosuke ; Fujita, Mayumi ; Azoulay-Shemer, Tamar ; Engineer, Cawas B. ; Kusumi, Kensuke ; Nishida, Ikuo ; Schroeder, Julian I. ; Iba, Koh. / Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 36. pp. 9038-9043.
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