Transcriptomic and evolutionary analysis of the mechanisms by which P. argentatum, a rubber producing perennial, responds to drought

Authors: NELSON, ANDREW - University Of Arizona; Ponciano, Grisel; McMahan, Colleen; ILUT, DANIEL - Cornell University; PUGH, N. - University Of Arizona; ELSHIKHA, DIAA - University Of Arizona; Hunsaker, Douglas - Doug; PAULI, DUKE - University Of Arizona

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2019
Publication Date: 11/13/2019
Citation: Nelson, A.D., Ponciano, G.P., McMahan, C.M., Ilut, D.C., Pugh, N.A., Elshikha, D.E., Hunsaker, D.J., Pauli, D. 2019. Transcriptomic and evolutionary analysis of the mechanisms by which P. argentatum, a rubber producing perennial, responds to drought. Biomed Central (BMC) Plant Biology. 19:494. https://doi.org/10.1186/s12870-019-2106-2.
DOI: https://doi.org/10.1186/s12870-019-2106-2

Interpretive Summary: For sustainable domestic natural rubber production in the United States, rubber-producing plants like guayule must continue to improve in yield and other characteristics. Since guayule is cultivated in the semi-arid southwestern United States, its response to and ability to survive heat and drought stress is paramount. State of the science tools, for example the genomics analyses used in this study, provide fundamental information regarding guayule’s response to drought at the gene expression level. Guayule survives drought stress by increasing the expression of defensive genes related to plant growth. The knowledge gained may aid in developing new varieties with even higher tolerance to arid conditions in the U.S. southwest.

Technical Abstract: Background: Guayule (Parthenium argentatum Gray) is a drought tolerant, rubber producing perennial shrub native to northern Mexico and the US Southwest. Hevea brasiliensis, currently the world’s only source of natural rubber, is grown as a monoculture, leaving it vulnerable to both biotic and abiotic stressors. Isolation of rubber from guayule occurs by mechanical harvesting of the entire plant. It has been reported that environmental conditions leading up to harvest have a profound impact on rubber yield. The link between rubber biosynthesis and drought, a common environmental condition in guayule’s native habitat, is currently unclear. Results: We took a transcriptomic and comparative genomic approach to determine how drought impacts rubber biosynthesis in guayule. We compared transcriptional profiles of stem tissue, the location of guayule rubber biosynthesis, collected from field-grown plants subjected to water-deficit (drought) and well-watered (control) conditions. Plants subjected to the imposed drought conditions displayed an increase in production of transcripts associated with defense responses and water homeostasis, and a decrease in transcripts associated with rubber biosynthesis. An evolutionary and comparative analysis of stress-response transcripts suggests that more anciently duplicated transcripts shared among the Asteraceae, rather than recently derived duplicates, are contributing to the drought response observed in guayule. In addition, we identified several deeply conserved long non-coding RNAs (lncRNAs) containing microRNA binding motifs. One lncRNA in particular, with origins at the base of Asteraceae, may be regulating the vegetative to reproductive transition observed in water-stressed guayule by acting as a miRNA sponge for miR166. Conclusions: These data represent the first genomic analyses of how guayule responds to drought like conditions in agricultural production settings. We identified an inverse relationship between stress-responsive transcripts and those associated with precursor pathways to rubber biosynthesis suggesting a physiological trade-off between maintaining homeostasis and plant productivity. We also identify a number of regulators of abiotic responses, including transcription factors and lncRNAs, that are strong candidates for future projects aimed at modulating rubber biosynthesis under water-limiting conditions common to guayules’ native production environment.