Abstract
Heterosis has been used widely in the breeding of maize and other crops and plays an important role in increasing yield, improving quality, and enhancing stress resistance, but its molecular mechanism is far from clear. To determine whether microRNA (miRNA)-dependent gene regulation is responsible for heterosis of elongating internodes below the ear and ear height in maize, a deep-sequencing strategy was applied to the elite hybrid Xundan20, which is currently cultivated widely in China, and its two parents. RNA was extracted from the eighth internode because it shows clear internode length heterosis. A total of 99 conserved maize miRNAs were detected in both the hybrid and parental lines. Most of these miRNAs were expressed nonadditively in the hybrid compared with its parental lines. These results indicated that miRNAs might participate in heterosis during internode expansion in maize and exert an influence on ear and plant height via the repression of their target genes. In total, eight novel miRNAs belonging to four miRNA families were predicted in the expanding internode. Global repression of miRNAs in the hybrid, which might result in enhanced gene expression, might be one reason why the hybrid shows longer internodes and taller seedlings compared with its parental lines.
Similar content being viewed by others
References
Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C et al (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62(2):250–264
Bowman JL (2004) Class III HD‐Zip gene regulation, the golden fleece of ARGONAUTE activity? Bioessays 26(9):938–942
Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs[J]. Science Signalling 320(5880):1185
Bruce AB (1910) The Mendelian Theory of Heredity and the Augmentation of Vigor. Science 32(827):627–628
Christianson JA, Wilson IW, Llewellyn DJ, Dennis ES (2009) The low-oxygen-induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low-oxygen treatment. Plant Physiol 149(4):1724–1738
Chuck G, Cigan AM, Saeteurn K et al (2007a) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39(4):544–549
Chuck G, Meeley R, Irish E et al (2007b) The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 39(12):1517–1521
Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137(8):1243–1250
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38
Ding D, Wang YJ, Han MS, Fu ZY, Li WH, Liu ZH, Hu YM, Tang JH (2012) MicroRNA transcriptomic analysis of heterosis during maize seed germination. PLoS One 7(6):e39578
Duvick DN (2001) Biotechnology in the 1930s: the development of hybrid maize. Nat Rev Genet 2(1):69–74
East EM (1936) Heterosis. Genetics 21(4):375–397
Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci U S A 99:9573–9578
Gao P, Bai X, Yang L, Lv D, Li Y, Cai H et al (2010) Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 231(5):991–1001
Guo M, Rupe MA, Zinselmeier C, Habben J et al (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16:1707–1716
Guo HS, **e Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down regulate auxin signals for arabidopsis lateral root development. Plant Cell 17(5):1376–1386
He G, Zhu X, Elling AA et al (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22(1):17–33
Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432
Hoecker N, Keller B, Muthreich N, Chollet D et al (2008) Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics 179:1275–1283
Hollick JB (2008) Sensing the epigenome. Trends Plant Sci 13:398–404
Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2:466–479
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Physiol Plant Mol Biol 57:19–53
Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36(1):94–104
Kulcheski FR, de Oliveira LFV, Molina LG et al (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12(1):307
Larièpe A, Mangin B, Jasson S, Combes V, Dumas F, Jamin P, Lariagon C, Jolivot D, Madur D, Fiévet J, Gallais A, Dubreuil P, Charcosset A, Moreau L (2012) The genetic basis of heterosis: multiparental quantitative trait loci map** reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.). Genetics 190:795–811
Leonardi A, Damerval C, Herbert Y, Gallais A, DeVienne D (1991) Association of protein amount polymorphisms (PAP) among maize lines with performances of their hybrids. Theor Appl Genet 82:552–560
Li WX, Oono Y, Zhu J, He XJ, Wu JM et al (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20(8):2238–2251
Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136(2):223–236
Liu Y, Von Behrens I, Muthreich N, Schütz W et al (2010) Regulation of the pericycle proteome in maize (Zea mays L.) primary roots by RUM1 which is required for lateral root initiation. Eur J Cell Biol 89:236–241
Liu Z, Kumari S, Zhang L, Zheng Y, Ware D (2012) Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS One 7(6):e39786
Mica E, Gianfranceschi L, Pè ME (2006) Characterization of five microRNA families in maize. J Exp Bot 57(11):2601–2612
Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17(3):705–721
Ogo Y, Kobayashi T, Nakanishi Itai R, Nakanishi H, Kakei Y et al (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283(19):13407–13417
Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ et al (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147
Paschold A, Marcon C, Hoecker N, Hochholdinger F (2009) Molecular dissection of heterosis manifestation during early maize root development. Theor Appl Genet 120:383–388
Powers L (1945) Relative yields of inbred lines and F1-hybrids of tomato. Bot Gaz 106:247–268
Ritchie SW, Hanway JJ, Benson GO (1989) How a corn plant develops. Iowa State University of Science and. Technology, Cooperative Extension Service
Romagnoli S, Maddaloni M, Livini C, Motto M (1990) Relationship between gene expression and hybrid vigor in primary root tips of young maize (Zea mays L.) plantlets. Theor Appl Genet 80:769–775
Shull GF (1952) Beginnings of the heterosis concept. Iowa State College Press, Ames, IA, pp 14–48
Siefers N, Dang KK, Kumimoto RW, Bynum WE, Tayrose G et al (2009) Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiol 149(2):625–641
Song R, Messing J (2003) Gene expression of a gene family in maize based on non-collinear haplotypes. Proc Natl Acad Sci U S A 100:9055–9060
Spray CR, Kobayashi M, Suzuki Y, Phinney BO, Gaskin P, MacMillan J (1996) The dwarf-1 (dt) Mutant of Zea mays blocks three steps in the gibberellin-biosynthetic pathway. Proc Natl Acad Sci U S A 93(19):10515–10518
Sunkar R, Jagadeeswaran G (2008) In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biology 8:13
Tang JH, Teng WT, Ma XQ, Yan JB, Meng YJ, Li JS (2007) The genetic dissection of plant height using a set of RIL population in maize. Euphytica 155:117–124
Teng F, Zhai L, Liu R, Bai W, Wang L, Huo D, Tao Y, Zheng Y, Zhang Z (2013) ZmGA3ox2, a candidate gene for a major QTL, qPH3.1, for plant height in maize. Plant J 73(3):405–416
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y et al (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16(9):2481–2498
Użarowska A, Keller B, Piepho HP et al (2007) Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height. Plant Mol Biol 63(1):21–34
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749
Wang Y, Hu Z, Yang Y, Chen X, Chen G (2009) Function annotation of an SBP-box gene in Arabidopsis based on analysis of co-expression networks and promoters. Int J Mol Sci 10(1):116–132
Wang QQ, Liu F, Chen XS, Ma XJ, Zeng HQ, Yang ZM (2010) Transcriptome profiling of early develo** cotton fiber by deep-sequencing reveals significantly differential expression of genes in a fuzzless/lintless mutant. Genomics 96(6):369–376
Wang JW, Park MY, Wang LJ, Koo Y, Chen XY et al (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7(2):e1002012. doi:10.1371/journal.pgen.1002012
Wang L, Gu XL, Xu DY, Wang W, Wang H et al (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 62(2):761–773
Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI et al (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143(4):1590–1600
Winkler RG, Helentjaris T (1995) The maize Dwarf3 gene encodes a cytochrome P450-mediated early step in Gibberellin biosynthesis. Plant Cell 7(8):1307–1317
**e Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14(23):3024–3036
**e Q, Guo HS, Dallman G, Fang S, Weissman AM et al (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419(6903):167–170
Yao YY, Guo GG, Ni ZF, Sunkar R, Du JK, Zhu JK, Sun QX (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8(6):R96
Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15(5):336–360
Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA (2006a) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63(2):246–254
Zhang BH, Pan XP, Cannon CH, Cobb GP, Anderson TA (2006b) Conservation and divergence of plant microRNA genes. Plant J 46(2):243–259
Zhang Y, Schwarz S, Saedler H, Huijser P (2007) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63(3):429–439
Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5(11):e1000716
Acknowledgments
This work was supported by the National High Technology Research and Development Program of China (2012AA10A305) and the Key Technologies R&D Program of China during the 12th 5-Year Plan period (2011BAD35B01).
Author information
Authors and Affiliations
Corresponding author
Additional information
Peng Zhao and Dong Ding contributed equally to this work
Rights and permissions
About this article
Cite this article
Zhao, P., Ding, D., Zhang, F. et al. Investigating the molecular genetic basis of heterosis for internode expansion in maize by microRNA transcriptomic deep sequencing. Funct Integr Genomics 15, 261–270 (2015). https://doi.org/10.1007/s10142-014-0411-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-014-0411-2