Light signals counteract alterations caused by simulated microgravity in proliferating plant cells.

Aránzazu Manzano,Raúl Herranz,F Javier Medina,Veronica Pereda‐Loth,Anne De Bures,Julio Sáez‐Vásquez

doi:10.1002/ajb2.1728

Abstract

Light and gravity are fundamental cues for plant development. Our understanding of the effects of light stimuli on plants in space, without gravity, is key to providing conditions for plants to acclimate to the environment. Here we tested the hypothesis that the alterations caused by the absence of gravity in root meristematic cells can be counteracted by light. Seedlings of wild-type Arabidopsis thaliana and two mutants of the essential nucleolar protein nucleolin (nuc1, nuc2) were grown in simulated microgravity, either under a white light photoperiod or under continuous darkness. Key variables of cell proliferation (cell cycle regulation), cell growth (ribosome biogenesis), and auxin transport were measured in the root meristem using in situ cellular markers and transcriptomic methods and compared with those of a 1 g control. The incorporation of a photoperiod regime was sufficient to attenuate or suppress the effects caused by gravitational stress at the cellular level in the root meristem. In all cases, values for variables recorded from samples receiving light stimuli in simulated microgravity were closer to values from the controls than values from samples grown in darkness. Differential sensitivities were obtained for the two nucleolin mutants. Light signals may totally or partially replace gravity signals, significantly improving plant growth and development in microgravity. Despite that, molecular alterations are still compatible with the expected acclimation mechanisms, which need to be better understood. The differential sensitivity of nuc1 and nuc2 mutants to gravitational stress points to new strategies to produce more resilient plants to travel with humans in new extraterrestrial endeavors.

Highlights

T (Molas and Kiss, 2009)
NUC1 is expressed at a high rate, mostly in proliferating tissues (Pontvianne et al, 2007), whereas the protein NUC2 plays a role in rDNA chromatin dynamics, preferentially at developmental transitions (Durut et al, 2014)
Seedlings of the Col‐0, nuc1, and nuc2 genotypes were grown for 6 days in vertical position (1 g control), either with photoperiod regime or dark conditions

Summary

Introduction

T (Molas and Kiss, 2009). Gravitropism and phototropism drive plant growth and development by producing opposite effects in the roots and in the aerial parts of the plant. Driven by tropistic cues, is supported by the activity of the meristematic tissues. The nucleolar protein nucleolin is the most abundant protein of exponentially growing cells and plays a major role in the regulation of ribosome biogenesis at different levels, namely, rDNA chromatin structure, rRNA gene transcription, pre‐rRNA processing and export of pre‐ ribosomal particles, and even in the structural organization of the nucleolus (Mongelard and Bouvet, 2007; Medina et al, 2010; Durut and Sáez‐Vásquez, 2015). In the case of light, specialized photoreceptor proteins—phytochromes—are modulators of cell proliferation and cell growth in meristems This modulation is different for the shoot and for the root meristematic cells, in agreement with the opposite phototropic behavior of the shoot and the root. Glucose binds to the central regulator TOR kinase inducing the activation of cell proliferation, through the expression of S‐phase genes, and ribosome biogenesis (Caldana et al, 2013; Xiong et al, 2013; Sablowski and Carnier Dornelas, 2014)

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