The mitochondrial protease AtFTSH4 safeguards Arabidopsis shoot apical meristem function

Abstract

The shoot apical meristem (SAM) ensures continuous plant growth and organogenesis. In LD 30 °C, plants lacking AtFTSH4, an ATP-dependent mitochondrial protease that counteracts accumulation of internal oxidative stress, exhibit a puzzling phenotype of premature SAM termination. We aimed to elucidate the underlying cellular and molecular processes that link AtFTSH4 with SAM arrest. We studied AtFTSH4 expression, internal oxidative stress accumulation, and SAM morphology. Directly in the SAM we analysed H2O2 accumulation, mitochondria behaviour, and identity of stem cells using WUS/CLV3 expression. AtFTSH4 was expressed in proliferating tissues, particularly during the reproductive phase. In the mutant, SAM, in which internal oxidative stress accumulates predominantly at 30 °C, lost its meristematic fate. This process was progressive and stage-specific. Premature meristem termination was associated with an expansion in SAM area, where mitochondria lost their functionality. All these effects destabilised the identity of the stem cells. SAM termination in ftsh4 mutants is caused both by internal oxidative stress accumulation with time/age and by the tissue-specific role of AtFTSH4 around the flowering transition. Maintaining mitochondria functionality within the SAM, dependent on AtFTSH4, is vital to preserving stem cell activity throughout development.

Learning To Breathe: Developmental Phase Transitions in Oxygen Status

“…. NO also appears to be required to maintain root meristem cell identity, as dependent on the auxin gradient [47], and two recent studies pointed to the importance of mitochondrial ROS homeostasis in cell-specific signalling, determining the identity of the root distal stem cells [48], and the maintenance of the shoot apical meristem [49]. These conclusions are in line with the general consensus that redox regulation is involved in multiple processes related to self-renewal and differentiation.…”

OPENER Is a Nuclear Envelope and Mitochondria Localized Protein Required for Cell Cycle Progression in Arabidopsis

“…One example is the Arabidopsis ATP-dependent zinc metalloprotease FtsH4, which is a mitochondrial inner membrane-integrated protease with proteolytic domains facing the intermembrane space. The ftsh4 mutant loses stem cell identity at elevated temperature (30°C), presumably due to accumulation of oxidatively damaged proteins (Dolzblasz et al, 2016(Dolzblasz et al, , 2018. Another example is Arabidopsis SLOW GROWTH3, which encodes a pentatricopeptide repeat protein for splicing of intron 2 of mitochondrial NADH dehydrogenase subunit 7 (NAD7) gene.…”

Regulation of Shoot Apical Meristem and Axillary Meristem Development in Plants

“…Reactive oxygen species (ROS) play essentials roles in plants [100][101][102]. The mutation of an ATP-dependent mitochondrial protease, AtFTSH4, leads to the accumulation of oxidative stress in SAM at 30 • C and affects meristematic fate [103]. promotes stem cell differentiation [104].…”