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Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana

The observation that plant roots skew in microgravity recently refuted the long-held conviction that skewing was a gravity-dependent phenomenon. Further, spaceflight root skewing suggests that specific root morphologies and cell wall remodeling systems may be important aspects of spaceflight physiol...

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Autores principales: Califar, Brandon, Sng, Natasha J., Zupanska, Agata, Paul, Anna-Lisa, Ferl, Robert J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7064724/
https://www.ncbi.nlm.nih.gov/pubmed/32194611
http://dx.doi.org/10.3389/fpls.2020.00239
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author Califar, Brandon
Sng, Natasha J.
Zupanska, Agata
Paul, Anna-Lisa
Ferl, Robert J.
author_facet Califar, Brandon
Sng, Natasha J.
Zupanska, Agata
Paul, Anna-Lisa
Ferl, Robert J.
author_sort Califar, Brandon
collection PubMed
description The observation that plant roots skew in microgravity recently refuted the long-held conviction that skewing was a gravity-dependent phenomenon. Further, spaceflight root skewing suggests that specific root morphologies and cell wall remodeling systems may be important aspects of spaceflight physiological adaptation. However, connections between skewing, cell wall modification and spaceflight physiology are currently based on inferences rather than direct tests. Therefore, the Advanced Plant Experiments-03-2 (APEX-03-2) spaceflight study was designed to elucidate the contribution of two skewing- and cell wall-associated genes in Arabidopsis to root behavior and gene expression patterns in spaceflight, to assess whether interruptions of different skewing pathways affect the overall spaceflight-associated process. SPIRAL1 is a skewing-related protein implicated in directional cell expansion, and functions by regulating cortical microtubule dynamics. SKU5 is skewing-related glycosylphosphatidylinositol-anchored protein of the plasma membrane and cell wall implicated in stress response signaling. These two genes function in different cellular pathways that affect skewing on the Earth, and enable a test of the relevance of skewing pathways to spaceflight physiological adaptation. In this study, both sku5 and spr1 mutants showed different skewing behavior and markedly different patterns of gene expression in the spaceflight environment. The spr1 mutant showed fewer differentially expressed genes than its Col-0 wild-type, whereas sku5 showed considerably more than its WS wild-type. Developmental age played a substantial role in spaceflight acclimation in all genotypes, but particularly in sku5 plants, where spaceflight 4d seedlings had almost 10-times as many highly differentially expressed genes as the 8d seedlings. These differences demonstrated that the two skewing pathways represented by SKU5 and SPR1 have unique and opposite contributions to physiological adaptation to spaceflight. The spr1 response is less intense than wild type, suggesting that the loss of SPR1 positively impacts spaceflight adaptation. Conversely, the intensity of the sku5 responses suggests that the loss of SKU5 initiates a much more complex, deeper and more stress related response to spaceflight. This suggests that proper SKU5 function is important to spaceflight adaptation.
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spelling pubmed-70647242020-03-19 Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana Califar, Brandon Sng, Natasha J. Zupanska, Agata Paul, Anna-Lisa Ferl, Robert J. Front Plant Sci Plant Science The observation that plant roots skew in microgravity recently refuted the long-held conviction that skewing was a gravity-dependent phenomenon. Further, spaceflight root skewing suggests that specific root morphologies and cell wall remodeling systems may be important aspects of spaceflight physiological adaptation. However, connections between skewing, cell wall modification and spaceflight physiology are currently based on inferences rather than direct tests. Therefore, the Advanced Plant Experiments-03-2 (APEX-03-2) spaceflight study was designed to elucidate the contribution of two skewing- and cell wall-associated genes in Arabidopsis to root behavior and gene expression patterns in spaceflight, to assess whether interruptions of different skewing pathways affect the overall spaceflight-associated process. SPIRAL1 is a skewing-related protein implicated in directional cell expansion, and functions by regulating cortical microtubule dynamics. SKU5 is skewing-related glycosylphosphatidylinositol-anchored protein of the plasma membrane and cell wall implicated in stress response signaling. These two genes function in different cellular pathways that affect skewing on the Earth, and enable a test of the relevance of skewing pathways to spaceflight physiological adaptation. In this study, both sku5 and spr1 mutants showed different skewing behavior and markedly different patterns of gene expression in the spaceflight environment. The spr1 mutant showed fewer differentially expressed genes than its Col-0 wild-type, whereas sku5 showed considerably more than its WS wild-type. Developmental age played a substantial role in spaceflight acclimation in all genotypes, but particularly in sku5 plants, where spaceflight 4d seedlings had almost 10-times as many highly differentially expressed genes as the 8d seedlings. These differences demonstrated that the two skewing pathways represented by SKU5 and SPR1 have unique and opposite contributions to physiological adaptation to spaceflight. The spr1 response is less intense than wild type, suggesting that the loss of SPR1 positively impacts spaceflight adaptation. Conversely, the intensity of the sku5 responses suggests that the loss of SKU5 initiates a much more complex, deeper and more stress related response to spaceflight. This suggests that proper SKU5 function is important to spaceflight adaptation. Frontiers Media S.A. 2020-03-04 /pmc/articles/PMC7064724/ /pubmed/32194611 http://dx.doi.org/10.3389/fpls.2020.00239 Text en Copyright © 2020 Califar, Sng, Zupanska, Paul and Ferl. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Califar, Brandon
Sng, Natasha J.
Zupanska, Agata
Paul, Anna-Lisa
Ferl, Robert J.
Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana
title Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana
title_full Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana
title_fullStr Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana
title_full_unstemmed Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana
title_short Root Skewing-Associated Genes Impact the Spaceflight Response of Arabidopsis thaliana
title_sort root skewing-associated genes impact the spaceflight response of arabidopsis thaliana
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7064724/
https://www.ncbi.nlm.nih.gov/pubmed/32194611
http://dx.doi.org/10.3389/fpls.2020.00239
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