Water-deficit responsive microRNAs in the primary root growth zone of maize

Authors: Seeve, Candace; SUNKAR, RAMANJULU - Oklahoma State University; ZHENG, YUN - Kunming University Of Science And Technology; LIU, LI - Kunming University Of Science And Technology; LIU, ZHIJIE - Huazhong Agricultural University; McMullen, Michael; Nelson, Sven; SHARP, ROBERT - University Of Missouri; Oliver, Melvin

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/12/2019
Publication Date: 10/24/2019
Publication URL: https://handle.nal.usda.gov/10113/6746338
Citation: Seeve, C.M., Sunkar, R., Zheng, Y., Liu, L., Liu, Z., Mcmullen, M.D., Nelson, S.K., Sharp, R.E., Oliver, M.J. 2019. Water-deficit responsive microRNAs in the primary root growth zone of maize. Biomed Central (BMC) Plant Biology. 19:447. https://doi.org/10.1186/s12870-019-2037-y.
DOI: https://doi.org/10.1186/s12870-019-2037-y

Interpretive Summary: Drought is the most important abiotic factor limiting maize productivity in the U.S and globally. Consequently, there is significant interest in identifying the genetic components, from the physiological to the molecular, that contribute to drought tolerance. Characterizing the gene regulatory networks that maintain maize root growth under water deficits would provide genetic targets to favorably manipulate a key drought tolerance trait and ultimately improve yield in drought conditions. Gene regulatory networks are primarily comprised of transcription factors (TFs) and regulatory small molecules that are nucleic acids (called micro-ribonucleic acids or miRNAs) both of which regulate how much a gene can influence the specific trait it is controlling, e.g. drought tolerance. Each works by enhancing or reducing the effectiveness of the gene product (transcript). In this study ARS researchers have identified the miRNAs that are made in maize primary roots in response to precise soil water deficits. The research also identified which genes the miRNAs regulate by degrading their transcripts. One of the miRNAs normally targets genes involved in regulating phosphate sensing and uptake from the soil, but under water deficit stress it appears that maize utilizes this miRNA in a different manner. The root protects the phosphate uptake gene transcripts by producing a decoy transcript that binds the miRNA and prevents the normal transcript from being degraded, thus protecting the phosphate status of the root. Understanding the involvement of miRNAs in regulating key root processes and growth during times when soil moisture is low will provide novel strategies for plant breeders to impact breeding efforts to improve root traits that mitigate the effect of drought on crop productivity.

Technical Abstract: MicroRNA-mediated gene regulatory networks play a significant role in plant growth and development and in environmental stress responses. In this study, small RNA sequencing revealed 79 microRNAs (miRNAs) and multiple miRNA variants (isomiRs) belonging to 26 microRNA families in the primary root growth zone of maize seedlings grown in vermiculite at one of three water potentials: well-watered (-0.02 MPa), mild water deficit stress (-0.3 MPa), and severe water deficit stress (-1.6 MPa). The abundance of 34 miRNAs belonging to 17 families was significantly different in severely water deficit-stressed primary root growth zone relative to well-watered primary root growth zone, and the abundance of 3 miRNAs was only significantly different in mildly water deficit-stress primary root growth zone relative to well-watered primary root growth zone (FDR < 0.05). Changes in miRNA abundance under water deficit stress were validated by stem loop RT-qPCR. Using degradome sequencing, 213 miRNA-regulated gene transcripts were identified in the primary root growth zone of maize seedlings exposed to the same treatment conditions. Trancriptome profiling indicated the water deficit-induced regulation (FDR < 0.05) of the abundance of 77 (miRNA-regulated) gene transcripts. One of the most strongly regulated miRNAs under both water deficit stress treatments was miR399e,i,j-3p implicating the possibility of nutrient deficiency during water deficit stress. However, at this early stage of seedling development the seed likely provides adequate nutrient resources for root growth raising the possibility that miR399e,i,j-3p plays a separate role in the water-deficit response. An uncharacterized maize transcript with high sequence complementarity to maize miR399 and that is similar to miR399 target mimics in other species was identified and was also differentially regulated by water deficit stress. It is hypothesized that this transcript is a miR399 target mimic and thus another regulatory player, moderating the role of miR399e,i,j-3p, in primary root growth zone water deficit responses.