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 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.
Highlights
Spaceflight studies offer unique insights into plant biological processes, and enable the exploration of the relationships between root morphology, gene expression and the physiological adaptation to spaceflight
Skewing trends can still be discerned by following the angles of growth as the roots develop, and these are quantified in Figure 2A for Col-0 and spr1, and in Figure 2B for WS and sku5
The physiological adaptation of sku5 to spaceflight is characterized by powerful stress responses, as well as the strong induction of late embryogenesis abundant (LEA) and other genes associated with seed development
Summary
Spaceflight studies offer unique insights into plant biological processes, and enable the exploration of the relationships between root morphology, gene expression and the physiological adaptation to spaceflight. A diversity of tropic gradients influence the path of growth in roots by initiating localized, asymmetrical changes in cell elongation These changes are primarily brought about through hormonal interactions and subsequent remodeling of cell physiology (Roy and Bassham, 2014; Vandenbrink et al, 2014; Schultz et al, 2017). Once thought to be a gravitydependent growth behavior (Oliva and Dunand, 2007), skewing occurs in the microgravity of spaceflight (Paul et al, 2012a). This suggests that skewing is independent of both the tropic force of gravity and the gravity-induced contact forces between roots and growth media (Millar et al, 2011; Paul et al, 2012a, 2013; Nakashima et al, 2014). The spaceflight environment provides a unique and relevant context in which to study genes associated with skewing phenotypes
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