Lipidomic insights into the response of Arabidopsis sepals to mild heat stress

Zican Chen; Weronika Jasinska; Muhammad Ashraf; Leah Rosental; Jung Hong; Dabing Zhang; Yariv Brotman; Jianxin Shi

doi:10.1007/s42994-023-00103-x

Lipidomic insights into the response of Arabidopsis sepals to mild heat stress

aBIOTECH. 2023 Jun 6;4(3):224-237. doi: 10.1007/s42994-023-00103-x. eCollection 2023 Sep.

Authors

Zican Chen^#¹, Weronika Jasinska^#², Muhammad Ashraf¹, Leah Rosental², Jung Hong¹, Dabing Zhang^{1

3

4}, Yariv Brotman², Jianxin Shi^{1

4}

Affiliations

¹ Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240 China.
² Department of Life Sciences, Ben Gurion University of the Negev, Beersheva, 84105 Israel.
³ School of Agriculture, Food and Wine, University of Adelaide, Urrbrae, SA 5064 Australia.
⁴ Yazhou Bay Institute of Deepsea Sci-Tech, Shanghai Jiao Tong University, Shanghai, 200240 China.

^# Contributed equally.

Abstract

Arabidopsis sepals coordinate flower opening in the morning as ambient temperature rises; however, the underlying molecular mechanisms are poorly understood. Mutation of one heat shock protein encoding gene, HSP70-16, impaired sepal heat stress responses (HSR), disrupting lipid metabolism, especially sepal cuticular lipids, leading to abnormal flower opening. To further explore, to what extent, lipids play roles in this process, in this study, we compared lipidomic changes in sepals of hsp70-16 and vdac3 (mutant of a voltage-dependent anion channel, VDAC3, an HSP70-16 interactor) grown under both normal (22 °C) and mild heat stress (27 °C, mild HS) temperatures. Under normal temperature, neither hsp70-16 nor vdac3 sepals showed significant changes in total lipids; however, vdac3 but not hsp70-16 sepals exhibited significant reductions in the ratios of all detected 11 lipid classes, except the monogalactosyldiacylglycerols (MGDGs). Under mild HS temperature, hsp70-16 but not vdac3 sepals showed dramatic reduction in total lipids. In addition, vdac3 sepals exhibited a significant accumulation of plastidic lipids, especially sulfoquinovosyldiacylglycerols (SQDGs) and phosphatidylglycerols (PGs), whereas hsp70-16 sepals had a significant accumulation of triacylglycerols (TAGs) and simultaneous dramatic reductions in SQDGs and phospholipids (PLs), such as phosphatidylcholines (PCs), phosphatidylethanolamines (PEs), and phosphatidylserines (PSs). These findings revealed that the impact of mild HS on sepal lipidome is influenced by genetic factors, and further, that HSP70-16 and VDAC3 differently affect sepal lipidomic responses to mild HS. Our studies provide a lipidomic insight into functions of HSP and VDAC proteins in the plant's HSR, in the context of floral development.

Supplementary information: The online version contains supplementary material available at 10.1007/s42994-023-00103-x.

Keywords: Floral development; Heat shock protein; Lipidomic profiling; Stress response; Voltage-dependent anion channel protein.