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 NimmakayalaEmail author
  • Umesh K. ReddyEmail author
Original Article


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.


Sweet potato Carbon dioxide Drought Field capacity microRNAs Photosynthesis 



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)


  1. Ainsworth EA (2008) Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Glob Chang Biol 14:1642–1650Google Scholar
  2. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372PubMedGoogle Scholar
  3. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedGoogle Scholar
  4. Ainsworth EA, Rogers A, Vodkin LO, Walter A, Schurr U (2006) The effects of elevated CO2 concentration on soybean gene expression. An analysis of growing and mature leaves. Plant Physiol 142:135–147PubMedPubMedCentralGoogle Scholar
  5. Akpinar BA, Budak H (2016) Dissecting miRNAs in wheat D genome progenitor, Aegilops tauschii. Front Plant Sci 7:606PubMedPubMedCentralGoogle Scholar
  6. Akpinar BA, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genomics 15:587–598PubMedGoogle Scholar
  7. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221PubMedGoogle Scholar
  8. Alptekin B, Langridge P, Budak H (2017) Abiotic stress miRNomes in the Triticeae. Funct Integr Genomics 17:145–170PubMedGoogle Scholar
  9. Arshad M, Mattsson J (2014) A putative poplar PP2C-encoding gene negatively regulates drought and abscisic acid responses in transgenic Arabidopsis thaliana. Trees 28:531–543Google Scholar
  10. Basson C, Groenewald J-H, Kossmann J, Cronjé C, Bauer R (2011) Upregulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in strawberry. Transgenic Res 20:925–931PubMedGoogle Scholar
  11. Baulcombe DJN (2004) RNA silencing in plants 431:356Google Scholar
  12. Bencze S, Bamberger Z, Janda T, Balla K, Varga B, Bedő Z, Veisz O (2014) Physiological response of wheat varieties to elevated atmospheric CO2 and low water supply levels. Photosynthetica 52:71–82Google Scholar
  13. Bian X, Ma P, Jia Z, Guo X, Xie Y (2016) Identification of miRNAs in sweet potato by Solexa sequencing. Russ J Plant Physiol 63:283–292Google Scholar
  14. Bloom AJ, Burger M, Kimball BA, Pinter PJ Jr (2014) Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat Clim Chang 4:477–480Google Scholar
  15. Bovell-Benjamin AC (2007) Sweet potato: a review of its past, present, and future role in human nutrition. In: Steve LT (ed) Advances in Food and Nutrition Research. Academic Press, pp. 1–59Google Scholar
  16. Budak H, Akpinar A (2011) Dehydration stress-responsive miRNA in Brachypodium distachyon: evident by genome-wide screening of microRNAs expression. Omics: A Journal of Integrative Biology 15:791–799PubMedGoogle Scholar
  17. Budak H, Khan Z, Kantar M (2014) History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Briefings in Functional Genomics 14:189–198PubMedGoogle Scholar
  18. Budak H, Kantar M, Bulut R, Akpinar BA (2015) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13PubMedGoogle Scholar
  19. Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70PubMedGoogle Scholar
  20. Cagirici HB, Alptekin B, Budak H (2017) RNA sequencing and co-expressed long non-coding RNA in modern and wild wheats. Sci Rep 7:10670PubMedPubMedCentralGoogle Scholar
  21. Candar-Cakir B, Arican E, Zhang B (2016) Small RNA and degradome deep sequencing reveals drought-and tissue-specific micrornas and their important roles in drought-sensitive and drought-tolerant tomato genotypes. Plant Biotechnol J 14:1727–1746PubMedPubMedCentralGoogle Scholar
  22. Chappelle EW, Kim MS, McMurtrey JE (1992) Ratio analysis of reflectance spectra (RARS): an algorithm for the remote estimation of the concentrations of chlorophyll a, chlorophyll b, and carotenoids in soybean leaves. Remote Sens Environ 39:239–247Google Scholar
  23. Chemura A, Mahoya C, Chidoko P, Kutywayo D Effect of soil moisture deficit stress on biomass accumulation of four coffee (Coffea arabica) varieties in Zimbabwe. ISRN Agronomy 2014, 2014:1–10Google Scholar
  24. De Souza AP, Gaspar M, Da Silva EA, Ulian EC, Waclawovsky AJ, Dos Santos RV, Teixeira MM, Souza GM, Buckeridge MS (2008) Elevated CO2 increases photosynthesis, biomass and productivity, and modifies gene expression in sugarcane. Plant Cell Environ 31:1116–1127PubMedGoogle Scholar
  25. Dehury B, Panda D, Sahu J, Sahu M, Sarma K, Barooah M, Sen P, Modi MK (2013) In silico identification and characterization of conserved miRNAs and their target genes in sweet potato (Ipomoea batatas L.) Expressed Sequence Tags (ESTs). Plant Signal Behav 8:e26543PubMedPubMedCentralGoogle Scholar
  26. Diaz J, Schmiediche P, Austin DF (1996) Polygon of crossability between eleven species of Ipomoea: section Batatas (Convolvulaceae). Euphytica 88:189–200. CrossRefGoogle Scholar
  27. Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077–3086PubMedGoogle Scholar
  28. Doupis G, Bertaki M, Psarras G, Kasapakis I, Chartzoulakis K (2013) Water relations, physiological behavior and antioxidant defence mechanism of olive plants subjected to different irrigation regimes. Sci Hortic 153:150–156Google Scholar
  29. Duan E, Wang Y, Liu L, Zhu J, Zhong M, Zhang H, Li S, Ding B, Zhang X, Guo X (2016) Pyrophosphate: fructose-6-phosphate 1-phosphotransferase (PFP) regulates carbon metabolism during grain filling in rice. Plant Cell Rep 35:1321–1331PubMedPubMedCentralGoogle Scholar
  30. Ferdous J, Sanchez-Ferrero JC, Langridge P, Milne L, Chowdhury J, Brien C, Tricker PJ (2016) Differential expression of microRNAs and potential targets under drought stress in barley. Plant, Cell & EnvironmentGoogle Scholar
  31. Flexas J, Bota J, Loreto F, Cornic G, Sharkey T (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279PubMedGoogle Scholar
  32. Fujimoto R, Taylor JM, Shirasawa S, Peacock WJ, Dennis ES (2012) Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc Natl Acad Sci 109:7109–7114PubMedGoogle Scholar
  33. Gajanayake B, Reddy KR (2016) Sweetpotato responses to mid-and late-season soil moisture deficits. Crop Sci 56:1865–1877Google Scholar
  34. Gajanayake B, Reddy KR, Shankle MW, Arancibia RA (2013) Early-season soil moisture deficit reduces sweetpotato storage root initiation and development. HortScience 48:1457–1462Google Scholar
  35. Gajanayake B, Reddy KR, Shankle MW, Arancibia RA (2014) Growth, developmental, and physiological responses of two sweetpotato (Ipomoea batatas L.[Lam]) cultivars to early season soil moisture deficit. Sci Hortic 168:218–228Google Scholar
  36. Ghannoum O, Sv C, Ziska L, Conroy JP (2000) The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant Cell Environ 23:931–942Google Scholar
  37. Gleadow RM, Evans JR, McCaffery S, Cavagnaro TR (2009) Growth and nutritive value of cassava (Manihot esculenta Cranz.) are reduced when grown in elevated CO2. Plant Biol 11:76–82PubMedGoogle Scholar
  38. Gunderson CA, Norby RJ, Wullschleger SD (2000) Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence. Tree Physiol 20:87–96PubMedGoogle Scholar
  39. Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for arabidopsis lateral root development. Plant Cell 17:1376–1386. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Guo R, Chen X, Lin Y, Xu X, Thu MK, Lai Z (2015) Identification of novel and conserved miRNAs in leaves of in vitro grown Citrus reticulata “Lugan” plantlets by solexa sequencing. Frontiers in plant science 6Google Scholar
  41. Hamza NB, Sharma N, Tripathi A, Sanan-Mishra N (2016) MicroRNA expression profiles in response to drought stress in Sorghum bicolor. Gene Expr Patterns 20:88–98PubMedGoogle Scholar
  42. Hewitt E (1966) Sand and water culture methods used in the study of plant nutrition, Commonwealth Bureau of Horticultural and Plantation Crops, East Mailing. Technical Communication 22Google Scholar
  43. Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429–3431PubMedPubMedCentralGoogle Scholar
  44. Hu J, Nakatani M, Lalusin AG, Kuranouchi T, Fujimura T (2003) Genetic analysis of sweetpotato and wild relatives using inter-simple sequence repeats (ISSRs). Breed Sci 53:297–304. CrossRefGoogle Scholar
  45. Hymus GJ, Baker NR, Long SP (2001) Growth in elevated CO2 can both increase and decrease photochemistry and photoinhibition of photosynthesis in a predictable manner. Dactylis glomerata grown in two levels of nitrogen nutrition. Plant Physiol 127:1204–1211PubMedPubMedCentralGoogle Scholar
  46. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014PubMedGoogle Scholar
  47. Jaleel CA, Manivannan P, Lakshmanan G, Gomathinayagam M, Panneerselvam R (2008) Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits. Colloids Surf B: Biointerfaces 61:298–303PubMedGoogle Scholar
  48. Jeong D-H, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. J Plant Biol 56:187–197Google Scholar
  49. Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484PubMedGoogle Scholar
  50. Kong L, Zhang Y, Ye Z-Q, Liu X-Q, Zhao S-Q, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349PubMedPubMedCentralGoogle Scholar
  51. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39:D152–D157. CrossRefPubMedGoogle Scholar
  52. Kulma A, Villadsen D, Campbell DG, Meek SE, Harthill JE, Nielsen TH, MacKintosh C (2004) Phosphorylation and 14-3-3 binding of Arabidopsis 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase. Plant J 37:654–667PubMedGoogle Scholar
  53. Landi S, Nurcato R, De Lillo A, Lentini M, Grillo S, Esposito S (2016) Glucose-6-phosphate dehydrogenase plays a central role in the response of tomato (Solanum lycopersicum) plants to short and long-term drought. Plant Physiol Biochem 105:79–89PubMedGoogle Scholar
  54. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876. CrossRefPubMedGoogle Scholar
  55. Li X-Q, Zhang D (2003) Gene expression activity and pathway selection for sucrose metabolism in developing storage root of sweet potato. Plant Cell Physiol 44:630–636PubMedGoogle Scholar
  56. Li P, Ainsworth EA, Leakey AD, Ulanov A, Lozovaya V, Ort DR, Bohnert HJ (2008a) Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated [CO2]. Plant Cell Environ 31:1673–1687PubMedGoogle Scholar
  57. Li R, Li Y, Kristiansen K, Wang J (2008b) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714PubMedGoogle Scholar
  58. Lichtenthaler HK (1987) [34] Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382Google Scholar
  59. Lin J-S, Lin C-C, Lin H-H, Chen Y-C, Jeng S-T (2012) MicroR828 regulates lignin and H2O2 accumulation in sweet potato on wounding. New Phytol 196:427–440PubMedGoogle Scholar
  60. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei Z, Clarke TH, Reed JW, Van Der Knaap E (2014) Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J Exp Bot 65:2507–2520PubMedPubMedCentralGoogle Scholar
  62. Liu S-C, Xu Y-X, Ma J-Q, Wang W-W, Chen W, Huang D-J, Fang J, Li X-J, Chen L (2016) Small RNA and degradome profiling reveals important roles for microRNAs and their targets in tea plant response to drought stress. Physiol Plant 158:435–451PubMedGoogle Scholar
  63. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ma H, Chen J, Zhang Z, Ma L, Yang Z, Zhang Q, Li X, Xiao J, Wang S (2017) MAPK kinase 10.2 promotes disease resistance and drought tolerance by activating different MAPKs in rice. Plant J 92:557–570PubMedGoogle Scholar
  65. Marschner H (2011) Marschner’s mineral nutrition of higher plants. Academic pressGoogle Scholar
  66. May P, Liao W, Wu Y, Shuai B, McCombie WR, Zhang MQ, Liu QA (2013) The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development. Nat Commun 4:2145PubMedGoogle Scholar
  67. Medina S, Vicente R, Amador A, Araus JL (2016) Interactive effects of elevated [CO2] and water stress on physiological traits and gene expression during vegetative growth in four durum wheat genotypes. Front Plant Sci 7Google Scholar
  68. Miao Z, Han Z, Zhang T, Chen S, Ma C (2017) A systems approach to a spatio-temporal understanding of the drought stress response in maize. Sci Rep 7:6590PubMedPubMedCentralGoogle Scholar
  69. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462PubMedGoogle Scholar
  70. Montes RAC, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, Marsch-Martínez N, Meyers BC, Green PJ, de Folter S (2014) Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun 5:3722Google Scholar
  71. Mullany LE, Herrick JS, Wolff RK, Slattery ML (2016) MicroRNA seed region length impact on target messenger RNA expression and survival in colorectal cancer. PLoS One 11:e0154177PubMedPubMedCentralGoogle Scholar
  72. Mutum RD, Kumar S, Balyan S, Kansal S, Mathur S, Raghuvanshi S (2016) Identification of novel miRNAs from drought tolerant rice variety Nagina 22. Sci Rep 6:30786PubMedPubMedCentralGoogle Scholar
  73. Negi S, Tak H, Ganapathi T (2018) A banana NAC transcription factor (MusaSNAC1) impart drought tolerance by modulating stomatal closure and H2O2 content. Plant Mol Biol 96:457–471PubMedGoogle Scholar
  74. Niu Y, Jin C, Jin G, Zhou Q, Lin X, Tang C, Zhang Y (2011) Auxin modulates the enhanced development of root hairs in Arabidopsis thaliana (L.) Heynh. under elevated CO2. Plant Cell Environ 34:1304–1317PubMedGoogle Scholar
  75. Nonami H (1998) Plant water relations and control of cell elongation at low water potentials. J Plant Res 111:373–382Google Scholar
  76. Pardales J Jr, Yamauchi A (2003) Regulation of root development in sweetpotato and cassava by soil moisture during their establishment periodRoots: the dynamic interface between plants and the earth. Springer, pp:201–208Google Scholar
  77. Pembleton KG, Sathish P (2014) Giving drought the cold shoulder: a relationship between drought tolerance and fall dormancy in an agriculturally important crop. AoB Plants 6Google Scholar
  78. Praba ML, Cairns J, Babu R, Lafitte H (2009) Identification of physiological traits underlying cultivar differences in drought tolerance in rice and wheat. J Agron Crop Sci 195:30–46Google Scholar
  79. Quan W, Liu X, Wang H, Chan Z (2016) Comparative physiological and transcriptional analyses of two contrasting drought tolerant alfalfa varieties. Front Plant Sci 6:1256PubMedPubMedCentralGoogle Scholar
  80. Reddy KR, Read JJ, McKinicn JM, Baker JJ, Tarpley L, Reddy VR (2001) Soil-plant-atmosphere-research (SPAR) facility: a tool for plant research and modeling. Biotronics 30:27–50Google Scholar
  81. Rolston LH, Clark CA, Cannon JM, Randle WM, Riley EG, Wilson PW, Robbins ML (1987) ‘Beauregard’ sweet potato. HortScience 22:1338–1339Google Scholar
  82. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527PubMedGoogle Scholar
  83. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292PubMedGoogle Scholar
  84. Springer CJ, Orozco RA, Kelly JK, Ward JK (2008) Elevated CO2 influences the expression of floral-initiation genes in Arabidopsis thaliana. New Phytol 178:63–67PubMedGoogle Scholar
  85. Stocker T, Dahe Q, Plattner G (2013) Climate change 2013: the physical science basis. In: Change IPoC (ed) Geneva, SwitzerlandGoogle Scholar
  86. Sun G, Stewart CN Jr, Xiao P, Zhang B (2012) MicroRNA expression analysis in the cellulosic biofuel crop switchgrass (Panicum virgatum) under abiotic stress. PLoS One 7:e32017PubMedPubMedCentralGoogle Scholar
  87. Sun R, Guo T, Cobb J, Wang Q, Zhang B (2015) Role of microRNAs during flower and storage root development in sweet potato. Plant Mol Biol Report 33:1731–1739Google Scholar
  88. Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. CrossRefPubMedPubMedCentralGoogle Scholar
  89. Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203PubMedGoogle Scholar
  90. Tadege M, Bucher M, Stähli W, Suter M, Dupuis I, Kuhlemeier C (1998) Activation of plant defense responses and sugar efflux by expression of pyruvate decarboxylase in potato leaves. Plant J 16:661–671Google Scholar
  91. Taub DR, Miller B, Allen H (2008) Effects of elevated CO2 on the protein concentration of food crops: a meta analysis. Glob Chang Biol 14:565–575Google Scholar
  92. Thiebaut F, Grativol C, Tanurdzic M, Carnavale-Bottino M, Vieira T, Motta MR, Rojas C, Vincentini R, Chabregas SM, Hemerly AS (2014) Differential sRNA regulation in leaves and roots of sugarcane under water depletion. PLoS One 9:e93822PubMedPubMedCentralGoogle Scholar
  93. Vicente R, Pérez P, Martínez-Carrasco R, Usadel B, Kostadinova S, Morcuende R (2015) Quantitative RT–PCR platform to measure transcript levels of C and N metabolism-related genes in durum wheat: transcript profiles in elevated [CO2] and high temperature at different levels of N supply. Plant Cell Physiol 56:1556–1573PubMedGoogle Scholar
  94. Villordon A, LaBonte D, Solis J, Firon N (2012) Characterization of lateral root development at the onset of storage root initiation in ‘Beauregard’ sweetpotato adventitious roots. HortScience 47:961–968Google Scholar
  95. Wall G, Brooks T, Adam N, Cousins A, Kimball B, Pinter P, LaMorte R, Triggs J, Ottman MJ, Leavitt S (2001) Elevated atmospheric CO2 improved sorghum plant water status by ameliorating the adverse effects of drought. New Phytol 152:231–248Google Scholar
  96. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138PubMedGoogle Scholar
  97. Wang T, Chen L, Zhao M, Tian Q, Zhang W-H (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:1PubMedPubMedCentralGoogle Scholar
  98. Ward J, Tissue DT, Thomas RB, Strain B (1999) Comparative responses of model C3 and C4 plants to drought in low and elevated CO2. Glob Chang Biol 5:857–867Google Scholar
  99. Wei R, Qiu D, Wilson IW, Zhao H, Lu S, Miao J, Feng S, Bai L, Wu Q, Tu D (2015) Identification of novel and conserved microRNAs in Panax notoginseng roots by high-throughput sequencing. BMC Genomics 16:835PubMedPubMedCentralGoogle Scholar
  100. Wu D-X, Wang G-X (2000) Interaction of CO2 enrichment and drought on growth, water use, and yield of broad bean (Vicia faba). Environ Exp Bot 43:131–139Google Scholar
  101. Wu H-J, Ma Y-K, Chen T, Wang M, Wang X-J (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Research:gks554Google Scholar
  102. Xie Q, Frugis G, Colgan D, Chua N-H (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036PubMedPubMedCentralGoogle Scholar
  103. Xie F, Stewart CN, Taki FA, He Q, Liu H, Zhang B (2014) High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol J 12:354–366PubMedGoogle Scholar
  104. Xu M, Hu T, Zhao J, Park M-Y, Earley KW, Wu G, Yang L, Poethig RS (2016) Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in Arabidopsis thaliana. PLoS Genet 12:e1006263PubMedPubMedCentralGoogle Scholar
  105. Yang J, Moeinzadeh M-H, Kuhl H, Helmuth J, Xiao P, Haas S, Liu G, Zheng J, Sun Z, Fan W (2017) Haplotype-resolved sweet potato genome traces back its hexaploidization history. Nature plants 3:696–703PubMedGoogle Scholar
  106. Yu N, Niu QW, Ng KH, Chua NH (2015) The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant J 83:673–685PubMedGoogle Scholar
  107. Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33:403–409. CrossRefPubMedGoogle Scholar
  108. Zhang N, Yang J, Wang Z, Wen Y, Wang J, He W, Liu B, Si H, Wang D (2014) Identification of novel and conserved microRNAs related to drought stress in potato by deep sequencing. PLoS One 9:e95489PubMedPubMedCentralGoogle Scholar
  109. Zhao X-Z, Wang G-X, Shen Z-X, Zhang H, Qiu M-Q (2006) Impact of elevated CO2 concentration under three soil water levels on growth of Cinnamomum camphora. J Zhejiang Univ Sci B 7:283–290PubMedPubMedCentralGoogle Scholar
  110. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168. CrossRefPubMedGoogle Scholar
  111. Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedPubMedCentralGoogle Scholar

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

Personalised recommendations