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Alterations in Redox Homeostasis and Profound Developmental Consequences Are at the Core of Sudden Gravity Change Responses of Sugarcane Plants

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Abstract

Understanding how abiotic stress influences plant development is important for crop development and management. The gravity changes force may reveal the additional details of the interconnected nature of plants’ stress-signaling pathways. Sugarcane plants were submitted to gravity-changing forces using the VSB-30 sounding rocket to identify how these plants respond to this abiotic stress using histological, biochemical, and molecular approaches to evaluate this response. The histological analysis allowed us to observe that this alteration culminates in the intense disorganization of vascular bundles and higher lignin accumulation in plant cell walls at the adaxial epidermis and the mesophyll cells. An increase in enzyme activity from superoxide dismutase and guaiacol peroxidase was also observed. Our results indicate that sugarcane’s response is similar to other abiotic stress responses, such as oxidative stress. The RNA sequencing data showed that these plantlets had a different expression on pathways associated with signal perception, plant metabolism involving photosynthesis, amino acid synthesis, cell division, DNA repair, and oxidative enzymes for scavenging ROS. These results presented here using sugarcane plantlets expand our knowledge of how plants can respond to the forces of gravity changes. The expression pattern in roots and leaves showed integrated and distinct responses for some known pathways, and both tissues expressed stress-related transcripts.

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Data Availability

Upon request,” RNA-seq data are available at BioProject ID PRJNA917241 (NCBI).

Abbreviations

AU:

Activity units

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid

BLAST:

Basic Local Alignment Search Tool

BP:

Biological processes

BUSCO:

Benchmarking Universal Single-Copy Orthologs

CAT:

Catalase

CC:

Cellular components

DAB:

Diaminobenzidine

GO:

Gene ontology

H2O2 :

Hydrogen peroxide

ISS:

International Space Station

KEGG:

Kyoto Encyclopedia of Genes and Genomes

LCH:

Leaves control in horizontal position

LCV:

Leaves control in vertical position

LMH:

Leaves VSB-30 flight-submitted in horizontal position

LMV:

Leaves VSB-30 flight-submitted in vertical position

MF:

Molecular functions

NO:

Nitric oxide

PCV:

Plantlets submitted to control shaker

POX:

Guaiacol peroxidase

RCH:

Roots control in horizontal position

RCV:

Roots control in vertical position

RIN:

RNA integrity number

RMH:

Roots VSB-30 flight-submitted in horizontal position

RMV:

Roots VSB-30 flight-submitted in vertical position

ROS:

Reactive oxygen species

SEM:

Scanning electron microscopy

SOD:

Superoxide dismutase

UniProtKB:

Entry from the UniProt database

g :

Earth gravity (normal condition)

g aM:

Sugarcane plant grown after microgravity

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Acknowledgements

We wish to express our gratitude to USINA ESTIVAS—BIOSEV for providing the sugarcane plants and to the teams from CLBI, CLA, and AEB for their invaluable support during the Maracati II mission. Additionally, we extend our thanks to Flávio Correia-Junior F. and Gualberto-Junior J., for the helpful suggestions and assistance in the development of the boxes utilized in the Maracati II mission. The authors would also like to acknowledge the technical support provided by the High-Performance Computing Center at UFRN (NPAD/UFRN).

Funding

“This research was funded by Agência Espacial Brasileira (AEB), FINEP, CAPES, Financial code 01; INCT- CNPQ/INESPAÇO. Helaine Cristiane Silva, Diego Gomes Teixeira, Vladmir Vieira do Nascimento; Kellya Francisca Mendonça Barreto were recipients of scholarship from CAPES; Katia C. Scortecci has a CNPq fellowship.”

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Authors

Contributions

HCS and KCS participated in the Maracati II mission, HCS and KFMB made the biochemical and histological assays; LFS, VVN, and DGT worked with RNA-seq data. KCS contributed to conceptualization and design of the work; KCS and JPMSS wrote a first draft of the manuscript; and all authors contributed to and agreed upon the final version.

Corresponding author

Correspondence to Katia Castanho Scortecci.

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On behalf of all authors, the corresponding author affirms that there is no conflict of interest.

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“Not applicable.”

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Handling Editor: Vijay Pratap Singh.

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Silva, L.F.d., Silva, H.C., Teixeira, D.G. et al. Alterations in Redox Homeostasis and Profound Developmental Consequences Are at the Core of Sudden Gravity Change Responses of Sugarcane Plants. J Plant Growth Regul 43, 920–939 (2024). https://doi.org/10.1007/s00344-023-11149-y

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  • DOI: https://doi.org/10.1007/s00344-023-11149-y

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