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

Abstract

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 skewingrelated protein implicated in directional cell expansion, and functions by regulating cortical microtubule dynamics. SKU5 is skewing-related glycosylphosphatidylinositolanchored 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.

Epigenomic Regulators Elongator Complex Subunit 2 and Methyltransferase 1 Differentially Condition the Spaceflight Response in Arabidopsis

“…The genes differentially expressed in response to spaceflight share similarities with many documented terrestrial responses. Hallmarks of spaceflight responses include differential expression of genes involved in pathways associated with cell wall remodeling, reactive oxygen species (ROS), pathogen attacks, wounding, salt stress, drought stress, and hormone signaling ( Hoson et al, 2002 ; Gao et al, 2008 ; Salmi and Roux, 2008 ; Blancaflor, 2013 ; Correll et al, 2013 ; Paul et al, 2013 ; Zupanska et al, 2013 ; Ferl et al, 2014 ; Inglis et al, 2014 ; Nakashima et al, 2014 ; Sugimoto et al, 2014 ; Kwon et al, 2015 ; Schüler et al, 2015 ; Zhang et al, 2015 ; Ferl and Paul, 2016 ; Herranz et al, 2019 ; Vandenbrink et al, 2019 ; Barker et al, 2020 ; Califar et al, 2020 ; Kruse et al, 2020 ; Angelos et al, 2021 ; Manian et al, 2021b ). Plants further respond to spaceflight with changes in DNA methylation, again similarly to the epigenetic effects that occur during terrestrial stresses.…”

“…DNA methylation and other epigenetic modifications have been reported to play a role in regulating the innate immune response and pathogen response ( Dowen et al, 2012 ; Wang et al, 2013 ; Yu et al, 2013 ; Tameshige et al, 2015 ; Jarosz et al, 2020 ). Many components of the gene networks associated with these pathogen-associated pathways are also differentially expressed by plants in spaceflight ( Correll et al, 2013 ; Paul et al, 2013 , 2017 ; Sugimoto et al, 2014 ; Kwon et al, 2015 ; Schüler et al, 2015 ; Herranz et al, 2019 ; Barker et al, 2020 ; Califar et al, 2020 ; Manian et al, 2021a ). This commonality of terrestrial environmental responses with spaceflight responses begged the question: do plants use similar tools to regulate genes in response to spaceflight?…”

An Integrative Study Showing the Adaptation to Sub-Optimal Growth Conditions of Natural Populations of Arabidopsis thaliana: A Focus on Cell Wall Changes

“…Although some trends are common to rosettes and floral stems upon growth at 22 °C or 15 °C, only two CW transcripts/CWPs of the oxido-reductases functional class were common to the short list of those differentially accumulated at a given growth temperature: AT5G15350 which is an early nodulin (AtEN22) homologous to blue copper binding proteins, and AT1G41830 which is a multicopper oxidase (AtSKS6) homologous to the A. thaliana SKU5 (SKEWED ROOT 5). To our knowledge, the role of the former protein has not been studied yet whereas SKU5 was shown to play a role in root directional growth [ 55 ] and more recently in the spaceflight response [ 56 ].…”

Interaction of light and gravity signals as a mechanism of counteracting alterations caused by simulated microgravity in proliferating plant cells

“…These include a complex network of processes including polar auxin transport and cytoskeletal dynamics [40,42]. A recent study in the ISS, using two mutants of skewing behavior, affecting different cellular functions, concludes that genes related to skewing could play a prominent role in plant space ight adaptation [43].…”