Spaceflight induces novel regulatory responses in Arabidopsis seedling as revealed by combined proteomic and transcriptomic analyses

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RESEARCH ARTICLE

Abstract

Background: Understanding of gravity sensing and response is critical to long-term human habitation in space and can provide new advantages for terrestrial agriculture. To this end, the altered gene expression profile induced by microgravity has been repeatedly queried by microarray and RNA-seq experiments to understand gravitropism. However, the quantification of altered protein abundance in space has been minimally investigated.

Results: Proteomic (iTRAQ-labelled LC-MS/MS) and transcriptomic (RNA-seq) analyses simultaneously quantified protein and transcript differential expression of three-day old, etiolated Arabidopsis thaliana seedlings grown aboard the International Space Station along with their ground control counterparts. Protein extracts were fractionated to isolate soluble and membrane proteins and analyzed to detect differentially phosphorylated peptides. In total, nine hundred sixty-eight RNAs, one hundred seven soluble proteins, and one hundred three membrane proteins were identified as differentially expressed. In addition, the proteomic analyses identified sixteen differential phosphorylation events. Proteomic data delivered novel insights and simultaneously provided new context to previously made observations of gene expression in microgravity. There is a sweeping shift in post-transcriptional mechanisms of gene regulation including RNA-decapping protein DCP5, the splicing factors GRP7 and GRP8, and AGO4. These data also indicate AHA2 and FERONIA as well as CESA1 and SHOU4 as central to the cell wall adaptations seen in spaceflight. Patterns of tubulin-alpha one, three, four and six phosphorylation further reveal an interaction of microtubule and redox homeostasis that mirrors osmotic response signaling elements. The absence of gravity also results in a seemingly wasteful dysregulation of plastid gene transcription. (Continued on next page)

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Conclusions: The datasets gathered from Arabidopsis seedlings exposed to microgravity revealed marked impacts on post-transcriptional regulation, cell wall synthesis, redox/microtubule dynamics, and plastid gene transcription. The impact of post-transcriptional regulatory alterations represents an unstudied element of the plant microgravity response with the potential to significantly impact plant growth efficiency and beyond. What's more, addressing the effects of microgravity on AHA2, CESA1, and alpha tubulins has the potential to enhance cytoskeletal organization and cell wall composition, thereby enhancing biomass production and growth in microgravity. Finally, understanding and manipulating the dysregulation of plastid gene transcription has further potential to address the goal of enhancing plant growth in the stressful conditions of microgravity.

Background

Results

Gene ontology analysis reveals processes altered in microgravity

Post-transcriptional gene regulation, alternative splicing, and post-translational modifications

Cell Wall synthesis in the spaceflight environment

Influences on plastid function and regulation

Altered redox state and ROS signaling

Discussion

Dysregulation of plastid transcripts

Global alterations to redox homeostasis

Cell Wall dynamics and Auxin on the ISS

Conclusions

Methods

Spaceflight parameters

RNA extraction and processing

Protein extraction and data analysis

Exclusions based on control experiments

Subcellular analyses

Gene ontology enrichment analyses

Overview

The study provides insights into how microgravity affects the regulatory mechanisms in Arabidopsis seedlings, highlighting novel post-transcriptional changes and their potential implications for plant growth efficiency in extraterrestrial environments.

Key Points

1Microgravity exposure leads to significant changes in gene expression and protein abundance in Arabidopsis seedlings
2Post-transcriptional regulation plays a crucial role in the plant's response to spaceflight conditions
3Proteomic and transcriptomic analyses reveal distinct regulatory shifts affecting cell wall synthesis and redox processes
4The research indicates potential strategies for enhancing plant growth in microgravity environments
5Understanding these regulatory responses could inform agricultural practices for space habitation and plant cultivation on Earth.

Details

Authors: Colin P. S. Kruse, Alexander D. Meyers, Proma Basu, Sarahann Hutchinson, Darron R. Luesse, Sarah E. Wyatt
Category: Biology and Natural Sciences

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