Involvement of Arabidopsis BIG protein in cell death mediated by Myo-inositol homeostasis

Quentin Bruggeman,Frédérique Tellier,Raphael Lugan,Florence Piron-Prunier,David Latrasse,Stéphanie Boutet-Mercey,Jean-Denis Faure,Sylvie Citerne,Cécile Raynaud,Moussa Benhamed,Marianne Delarue,Christelle Mazubert,Deborah Manza-Mianza,Catherine Bergounioux

doi:10.1038/s41598-020-68235-4

Abstract

Programmed cell death (PCD) is essential for several aspects of plant life. We previously identified the mips1 mutant of Arabidopsis thaliana, which is deficient for the enzyme catalysing myo-inositol synthesis, and that displays light-dependent formation of lesions on leaves due to Salicylic Acid (SA) over-accumulation. Rationale of this work was to identify novel regulators of plant PCD using a genetic approach. A screen for secondary mutations that abolish the mips1 PCD phenotype identified a mutation in the BIG gene, encoding a factor of unknown molecular function that was previously shown to play pleiotropic roles in plant development and defence. Physiological analyses showed that BIG is required for lesion formation in mips1 via SA-dependant signalling. big mutations partly rescued transcriptomic and metabolomics perturbations as stress-related phytohormones homeostasis. In addition, since loss of function of the ceramide synthase LOH2 was not able to abolish cell death induction in mips1, we show that PCD induction is not fully dependent of sphingolipid accumulation as previously suggested. Our results provide further insights into the role of the BIG protein in the control of MIPS1-dependent cell death and also into the impact of sphingolipid homeostasis in this pathway.

Highlights

IntroductionWe previously identified the mips[1] mutant of Arabidopsis thaliana, which is deficient for the enzyme catalysing myo-inositol synthesis, and that displays light-dependent formation of lesions on leaves due to Salicylic Acid (SA) over-accumulation
Programmed cell death (PCD) is essential for several aspects of plant life
We demonstrated an epistatic relationship between mips[1] and big mutations and that PCD triggered by a decrease in MI content can be reverted by the big mutation, possibly through the suppression of Salicylic Acid (SA) production

Summary

Introduction

We previously identified the mips[1] mutant of Arabidopsis thaliana, which is deficient for the enzyme catalysing myo-inositol synthesis, and that displays light-dependent formation of lesions on leaves due to Salicylic Acid (SA) over-accumulation. A screen for secondary mutations that abolish the mips[1] PCD phenotype identified a mutation in the BIG gene, encoding a factor of unknown molecular function that was previously shown to play pleiotropic roles in plant development and defence. Since loss of function of the ceramide synthase LOH2 was not able to abolish cell death induction in mips[1], we show that PCD induction is not fully dependent of sphingolipid accumulation as previously suggested. It has been observed that the cell death phenotype of mips[1] mutant correlated with elevated levels of ceramides and hydroxyceramides, likely because the conversion of ceramides in inositol phosphoryl ceramide is compromised in this mutant due to the inhibition of MI production[7]

Methods

Findings

Conclusion