HSFA2 Functions in the Physiological Adaptation of Undifferentiated Plant Cells to Spaceflight

Abstract

Heat Shock Factor A2 (HsfA2) is part of the Heat Shock Factor (HSF) network, and plays an essential role beyond heat shock in environmental stress responses and cellular homeostatic control. Arabidopsis thaliana cell cultures derived from wild type (WT) ecotype Col-0 and a knockout line deficient in the gene encoding HSFA2 (HSFA2 KO) were grown aboard the International Space Station (ISS) to ascertain whether the HSF network functions in the adaptation to the novel environment of spaceflight. Microarray gene expression data were analyzed using a two-part comparative approach. First, genes differentially expressed between the two environments (spaceflight to ground) were identified within the same genotype, which represented physiological adaptation to spaceflight. Second, gene expression profiles were compared between the two genotypes (HSFA2 KO to WT) within the same environment, which defined genes uniquely required by each genotype on the ground and in spaceflight-adapted states. Results showed that the endoplasmic reticulum (ER) stress and unfolded protein response (UPR) define the HSFA2 KO cells’ physiological state irrespective of the environment, and likely resulted from a deficiency in the chaperone-mediated protein folding machinery in the mutant. Results further suggested that additional to its universal stress response role, HsfA2 also has specific roles in the physiological adaptation to spaceflight through cell wall remodeling, signal perception and transduction, and starch biosynthesis. Disabling HsfA2 altered the physiological state of the cells, and impacted the mechanisms induced to adapt to spaceflight, and identified HsfA2-dependent genes that are important to the adaption of wild type cells to spaceflight. Collectively these data indicate a non-thermal role for the HSF network in spaceflight adaptation.

Test of Arabidopsis Space Transcriptome: A Discovery Environment to Explore Multiple Plant Biology Spaceflight Experiments

“…Thus, Zupanska et al (2013) compared Arabidopsis seedlings and wild type cell cultures grown in the dark within the BRIC. Subsequent spaceflight experiments saw comparisons between wild-type Arabidopsis cell cultures and those with mutations in the genes for ALTERED RESPONSE TO GRAVITY 1 (ARG1; a well-studied Arabidopsis gene related to gravity sensing) and HEAT SHOCK FACTOR 2a [HSF2a; a key heat shock response-related transcriptional regulator; (Zupanska et al, 2017;Zupanska et al, 2019)]. Fengler et al (2015) also flew Arabidopsis and rice cell cultures in the SIMBOX hardware on the Shenzhou-8 spacecraft.…”

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

“…Several classes of stress response genes have been identified as consistently involved in the response to spaceflight across ecotypes of Arabidopsis via analyses of gene expression. Heat shock genes are often induced by spaceflight (Paul et al, 2005(Paul et al, , 2012bSalmi and Roux, 2008;Shagimardanova et al, 2010;Zupanska et al, 2013Zupanska et al, , 2017Zupanska et al, , 2019Johnson et al, 2017;Choi et al, 2019). Reactive oxygen species (ROS) signaling and scavenging processes are also common in the spaceflight response, though ROS-associated genes have been observed as both up-and downregulated in spaceflight Abbreviations: d, day; DEG, differentially expressed gene; FLT, spaceflight; GC, ground control; GO, gene ontology; GPI-AP, glycosylphosphatidylinositolanchored protein.…”

“…Mutations in genes associated with stress response and signaling pathways can significantly alter the differential gene expression profiles of spaceflight physiological adaptation. Single gene mutations in heat shock transcription factors, gravity perception genes, and light signaling genes in Arabidopsis seedlings and cultures exhibit altered spaceflight responses Zupanska et al, 2017Zupanska et al, , 2019. Therefore, we sought to understand better the relationships among spaceflight responses, root morphology, and spaceflight adaptation by exploring the spaceflight responses of two single gene skewing-related mutant lines: spiral1 and sku5.…”

Rocket Science: The Effect of Spaceflight on Germination Physiology, Ageing, and Transcriptome of Eruca sativa Seeds

“…Laboratories inside spaceships in low Earth orbit (LEO) have enabled investigations of the effects of long-term microgravity and helped, for example, to unravel mechanisms underpinning plant tropisms that would otherwise be masked by the effects of gravitropism [2,9]. Molecular analysis of growing seedlings and adult plants in microgravity by epigenomics [10], transcriptomics, and proteomics [8,9,11] identified known and novel genes specific for the response to the space environment. This research has potential to be applied to growing fresh food derived from plants for nutrition and human survival in space during long-distance space travel [5,7,[12][13][14][15][16][17].…”