Abstract
Key message
High-throughput sequencing and subsequent analysis indicated that miRNAs play crucial roles in floral thermogenesis of Magnolia denudata flowers.
Abstract
Animal-like thermogenic activity in flowers has been reported in several families of seed plants. Many studies have explored the ecological significance of thermogenesis in pollination biology; however, the molecular mechanisms regulating floral thermogenesis remain unclear. To characterize the roles of miRNA in floral thermogenesis, we analyzed miRNA expression in Magnolia denudata flowers during thermogenic and non-thermogenic stages. High-throughput sequencing and subsequent analysis revealed 82 conserved and 32 novel miRNAs in M. denudata flowers. A total of 187 EST sequences were predicted to be targets of 63 miRNAs. The target genes fell into 15 KOG functional classes and were involved in 25 KEGG pathways, suggesting that miRNAs play extensive regulatory roles in biological processes of M. denudata flowers. Among the identified miRNAs, 17 were differentially expressed between thermogenic and non-thermogenic stages and thus were thought to play roles in regulating floral thermogenesis in M. denudata. GO enrichment analysis revealed that target genes of these thermogenesis-related miRNAs were enriched in the functional groups ‘polyprenyl transferase activity’ and ‘photosynthetic electron transport’. Considering the important roles of polyprenyl transferase in the respiratory chain and the fact that floral thermogenesis of M. denudata flowers is associated with sunlight, we can infer that miRNAs play crucial roles in floral thermogenesis of M. denudata flowers by regulating cellular respiration and light reactions.
Similar content being viewed by others
References
Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769
Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455:64–71
Bartel DP (2004) microRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159
Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077–3086
Forsgren M, Attersand A, Lake S, Grunler J, Swiezewska E, Dallner G, Climent I (2004) Isolation and functional expression of human CoQ2, a gene encoding a polyprenyl transferase involved in the synthesis of CoQ. Biochem J 382:519–526
Gottsberger G, Amaral A (1984) Pollination strategies in Brazilian philodendron species. Ber deut bot Ges 97:391–410
Ito-Inaba Y, Sato M, Masuko H, Hida Y, Toyooka K, Watanabe M, Inaba T (2009) Developmental changes and organelle biogenesis in the reproductive organs of thermogenic skunk cabbage (Symplocarpus renifolius). J Exp Bot 60:3909–3922
Ito-Inaba Y, Hida Y, Matsumura H, Masuko H, Yazu F, Terauchi R, Watanabe M, Inaba T (2012) The gene expression landscape of thermogenic skunk cabbage suggests critical roles for mitochondrial and vacuolar metabolic pathways in the regulation of thermogenesis. Plant Cell Environ 35:554–566
Kakizaki Y, Moore AL, Ito K (2012) Different molecular bases underlie the mitochondrial respiratory activity in the homoeothermic spadices of Symplocarpus renifolius and the transiently thermogenic appendices of Arum maculatum. Biochem J 445:237–246
Kitao N, Hashimoto M (2012) Increased thermogenic capacity of brown adipose tissue under low temperature and its contribution to arousal from hibernation in Syrian hamsters. Am J Physiol Regul Integr Comp Physiol 302:R118–R125
Li JK, Huang SQ (2009) Flower thermoregulation facilitates fertilization in Asian sacred lotus. Ann Bot 103:1159–1163
Liu P, Yan K, Lei YX, Xu R, Zhang YM, Yang GD, Huang JG, Wu CA, Zheng CC (2013) Transcript profiling of microRNAs during the early development of the maize brace root via Solexa sequencing. Genomics 101:149–156
Luevano-Martinez LA (2012) Uncoupling proteins (UCP) in unicellular eukaryotes: true UCPs or UCP1-like acting proteins? FEBS Lett 586:1073–1078
Luo Y, Guo Z, Li L (2013) Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev Biol 380:133–144
Meeuse BD, Raskin I (1988) Sexual reproduction in the arum lily family, with emphasis on thermogenicity. Sex Plant Reprod 1:3–15
Miller RE, Grant NM, Giles L, Ribas-Carbo M, Berry JA, Watling JR, Robinson SA (2011) In the heat of the night—alternative pathway respiration drives thermogenesis in Philodendron bipinnatifidum. New Phytol 189:1013–1026
Mohorianu I, Schwach F, Jing R, Lopez-Gomollon S, Moxon S, Szittya G, Sorefan K, Moulton V, Dalmay T (2011) Profiling of short RNAs during fleshy fruit development reveals stage-specific sRNAome expression patterns. Plant J 67:232–246
Puzey JR, Karger A, Axtell M, Kramer EM (2012) Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS One 7:e33034
Quinzii C, Naini A, Salviati L, Trevisson E, Navas P, DiMauro S, Hirano M (2006) A mutation in para-hydroxybenzoate-polyprenyl transferase (CoQ2) causes primary coenzyme Q10 deficiency. Am J Hum Genet 78:345–349
Romanel E, Silva TF, Correa RL, Farinelli L, Hawkins JS, Schrago CE, Vaslin MF (2012) Global alteration of microRNAs and transposon-derived small RNAs in cotton (Gossypium hirsutum) during cotton leafroll dwarf polerovirus (CLRDV) infection. Plant Mol Biol 80:443–460
Seymour RS (2010) Scaling of heat production by thermogenic flowers: limits to floral size and maximum rate of respiration. Plant Cell Environ 33:1474–1485
Seymour RS, Schultze-Motel P (1996) Thermoregulating lotus flowers. Nature 383:305
Seymour RS, Schultze-Motel P (1998) Physiological temperature regulation by flowers of the sacred lotus. Philos Trans R Soc Lond B Biol Sci 353:935–943
Seymour RS, White CR, Gibernau M (2003) Environmental biology: heat reward for insect pollinators. Nature 426:243–244
Seymour RS, Maass E, Bolin JF (2009a) Floral thermogenesis of three species of Hydnora (Hydnoraceae) in Africa. Ann Bot 104:823–832
Seymour RS, Gibernau M, Pirintsos SA (2009b) Thermogenesis of three species of Arum from Crete. Plant Cell Environ 32:1467–1476
Seymour RS, Ito Y, Onda Y, Ito K (2009c) Effects of floral thermogenesis on pollen function in Asian skunk cabbage Symplocarpus renifolius. Biol Lett 5:568–570
Seymour RS, Silberbauer-Gottsberger I, Gottsberger G (2010) Respiration and temperature patterns in thermogenic flowers of Magnolia ovata under natural conditions in Brazil. Funct Plant Biol 37:870–878
Suinyuy TN, Donaldson JS, Johnson SD (2013) Patterns of odour emission, thermogenesis and pollinator activity in cones of an African cycad: what mechanisms apply? Ann Bot 112:891–902
Thien LB, Bernhardt P, Devall MS, Chen ZD, Luo YB, Fan JH, Yuan LC, Williams JH (2009) Pollination biology of basal angiosperms (ANITA grade). Am J Bot 96:166–182
Wang RH, Jia H, Wang JZ, Zhang ZX (2010) Flowering and pollination patterns of Magnolia denudata with emphasis on anatomical changes in ovule and seed development. Flora 205:259–265
Wang ZJ, Huang JQ, Huang YJ, Li Z, Zheng BS (2012) Discovery and profiling of novel and conserved microRNAs during flower development in Carya cathayensis via deep sequencing. Planta 236:613–621
Wang RH, Liu XY, Mou SL, Xu S, Zhang ZX (2013) Temperature regulation of floral buds and floral thermogenicity in Magnolia denudata (Magnoliaceae). Trees 27:1755–1762
Watling JR, Robinson SA, Seymour RS (2006) Contribution of the alternative pathway to respiration during thermogenesis in flowers of the sacred lotus. Plant Physiol 140:1367–1373
Xia NH, Liu YH, Nooteboom HP (2008) Magnoliaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis, pp 48–90
Zhai J, Zhao Y, Simon SA, Huang S, Petsch K, Arikit S, Pillay M, Ji L, Xie M, Cao X, Yu B, Timmermans M, Yang B, Chen X, Meyers BC (2013) Plant microRNAs display differential 3′ truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species. Plant Cell 25:2417–2428
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Author contribution statement
XL, DC, and RW conceived and designed the experiments; XL, DC, and XJ performed the experiments; XL, DC, ZZ, YW, and RW analyzed the data; XL, DC, and RW wrote the paper.
Acknowledgments
This work was supported by the Fundamental Research Funds for Central Universities (No. YX 2014-14) and National Science Fund of China (No. 31100450 & No. J1103516).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. D. Guy.
X. Liu and D. Cao contributed equally to the manuscript.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary material 1 (PDF 43 kb)
Figure S1. Work flow of ACGT-101.
Supplementary material 2 (PDF 44 kb)
Table S1. Detailed information for conserved miRNAs.
Supplementary material 3 (PDF 37 kb)
Table S2. Detailed information for novel miRNAs.
Supplementary material 4 (PDF 47 kb)
Table S3. Predicted targets of identified miRNAs.
Supplementary material 5 (PDF 39 kb)
Table S4. Differentially expressed miRNAs in pistils at bud swelling and female stage flowers.
Supplementary material 6 (PDF 38 kb)
Table S5. Differentially expressed miRNAs in pistils at bud swelling and male stage flowers.
Supplementary material 7 (PDF 34 kb)
Table S6. Putative targets of thermogenesis-related miRNAs.
Rights and permissions
About this article
Cite this article
Liu, X., Cao, D., Ji, X. et al. miRNAs play essential roles in the floral thermogenesis of Magnolia denudata (Magnoliaceae). Trees 29, 35–42 (2015). https://doi.org/10.1007/s00468-014-1051-9
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1007/s00468-014-1051-9