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Functional & Integrative Genomics

, Volume 19, Issue 1, pp 171–190 | Cite as

Elevated carbon dioxide and drought modulate physiology and storage-root development in sweet potato by regulating microRNAs

  • Thangasamy Saminathan
  • Alejandra Alvarado
  • Carlos Lopez
  • Suhas Shinde
  • Bandara Gajanayake
  • Venkata L. Abburi
  • Venkata G. Vajja
  • Guru Jagadeeswaran
  • K. Raja Reddy
  • Padma Nimmakayala
  • Umesh K. Reddy
Original Article

Abstract

Elevated CO2 along with drought is a serious global threat to crop productivity. Therefore, understanding the molecular mechanisms plants use to protect these stresses is the key for plant growth and development. In this study, we mimicked natural stress conditions under a controlled Soil-Plant-Atmosphere-Research (SPAR) system and provided the evidence for how miRNAs regulate target genes under elevated CO2 and drought conditions. Significant physiological and biomass data supported the effective utilization of source-sink (leaf to root) under elevated CO2. Additionally, elevated CO2 partially rescued the effect of drought on total biomass. We identified both known and novel miRNAs differentially expressed during drought, CO2, and combined stress, along with putative targets. A total of 32 conserved miRNAs belonged to 23 miRNA families, and 25 novel miRNAs were identified by deep sequencing. Using the existing sweet potato genome database and stringent analyses, a total of 42 and 22 potential target genes were predicted for the conserved and novel miRNAs, respectively. These target genes are involved in drought response, hormone signaling, photosynthesis, carbon fixation, sucrose and starch metabolism, etc. Gene ontology and KEGG ontology functional enrichment revealed that these miRNAs might target transcription factors (MYB, TCP, NAC), hormone signaling regulators (ARF, AP2/ERF), cold and drought factors (corA), carbon metabolism (ATP synthase, fructose-1,6-bisphosphate), and photosynthesis (photosystem I and II complex units). Our study is the first report identifying targets of miRNAs under elevated CO2 levels and could support the molecular mechanisms under elevated CO2 in sweet potato and other crops in the future.

Keywords

Sweet potato Carbon dioxide Drought Field capacity microRNAs Photosynthesis 

Notes

Acknowledgements

Funding support is provided to Dr. Nimmakayala by USDA-NIFA (proposal no: 2005-03605). We also thank the USDA–NIFA specialty crop research initiative (grant no. 2009-51181-06071) and the USDA–NIFA (grant no. 2013-34263-20931) sub-award to Mississippi State University (no. G-7799-2).

Author contributions

UR, PN, and KRR conceived the idea and designed the work. KRR and BG performed SPAR experiments and collected. KRR, BG, and CL analyzed the SPAR data. TS, AA, and VLA extracted small RNAs. CL performed bioinformatic analysis of small RNAs. TS, AA, VGV, and CL validated miRNAs by using stem-loop RT-qPCR. TS, AA, SS, GJ, KRR, and UKR drafted the manuscript. PN, SS, TS, GJ, and UKR critically reviewed the manuscript. All authors approved the final version of the manuscript.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.

Supplementary material

10142_2018_635_MOESM1_ESM.jpg (1.4 mb)
Fig S1 Secondary structures of novel miRNAs. Characteristic hairpin structures of novel miRNA precursors for selected novel miRNAs found in sweet potato. The regions of mature miRNAs and passenger miRNAs are highlighted. Portions of the large folding structure were trimmed for alignment. (JPG 1450 kb)
10142_2018_635_MOESM2_ESM.jpg (858 kb)
Fig S2 First nucleotide bias position of miRNAs. First nucleotide bias of sRNA reads with drought and CO2 stress. The horizontal coordinates are length of novel miRNAs and the vertical coordinates are percentage of AUCG at the first base. (JPG 857 kb)
10142_2018_635_MOESM3_ESM.jpg (1.7 mb)
Fig S3 Nucleotide bias at each position of sRNA reads with drought and CO2 stress. The horizontal coordinates are each position of sRNA reads and the vertical coordinates are percentage of AUCG at each base. (JPG 1700 kb)
10142_2018_635_MOESM4_ESM.jpg (2.2 mb)
Fig S4 KEGG pathways of target genes involved in carbon fixation, oxidative phosphorylation, photosynthesis, starch and sucrose metabolism, and plant hormone signal transduction. (JPG 2234 kb)
10142_2018_635_MOESM5_ESM.pdf (157 kb)
Fig S5 KEGG pathways showing participation of miRNA target genes in carbon fixation, plant hormone signaling, photosynthesis, and sucrose and starch metabolism. (PDF 157 kb)
10142_2018_635_MOESM6_ESM.docx (30 kb)
Table S1 (DOCX 30 kb)
10142_2018_635_MOESM7_ESM.xlsx (16 kb)
Table S2 (XLSX 15 kb)
10142_2018_635_MOESM8_ESM.docx (31 kb)
Table S3 (DOCX 31 kb)
10142_2018_635_MOESM9_ESM.docx (30 kb)
Table S4 (DOCX 30 kb)
10142_2018_635_MOESM10_ESM.xlsx (11 kb)
Table S5 (XLSX 11 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Gus R. Douglass Institute and Department of BiologyWest Virginia State UniversityInstituteUSA
  2. 2.Department of Plant and Soil SciencesMississippi State UniversityStarkvilleUSA
  3. 3.Department of Biochemistry and Molecular BiologyOklahoma State UniversityStillwaterUSA

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