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Systematic identification and characterization of candidate genes for the regulation of plant height in maize

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Abstract

Plant height, which is an important trait for maize breeding because of its relationship with lodging resistance and yield production, is reportedly determined by multiple qualitative and quantitative genes. However, only a few plant height-related genes have been cloned or characterized in maize. In the present study, previously characterized genes involved in the regulation of plant height were collected from maize, Arabidopsis thaliana, Oryza sativa and sorghum. A collinearity analysis was subsequently performed to identify homologs in the maize genome. A total of 82 new homologous genes were identified as possibly influencing plant height in maize. Interestingly, most of the candidates were involved in the synthesis or signaling of various phytohormones, particularly gibberellin (GA), implying that phytohormones are critical for regulating plant height. Moreover, in a comprehensive analysis of the expression patterns for these genes, substantial variability was observed across tissues and developmental stages, and each tissue exhibited diverse gene expression patterns. An RNA-sequencing analysis of tall and dwarf inbred lines revealed that 15 candidates were differentially expressed, among which six (40.0%) genes were functionally characterized as affecting various phytohormone pathways. Furthermore, the expression of candidate genes potentially involved in the GA signaling pathway was strongly induced by an exogenous GA treatment. This increased expression may have contributed to the observed faster growth rate of the GA-treated plants compared with the mock controls. Our results indicate that the spatial or temporal expression of genes involved in various phytohormone pathways may be associated with the regulation of plant height in maize.

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References

  • Ashikari M, Sasaki A, Ueguchi-Tanaka M, Itoh H, Nishimura A, Datta S, Ishiyama K, Saito T, Kobayashi M, Khush GS (2002) Loss-of-function of a Rice Gibberellin Biosynthetic Gene, GA2O oxidase (GA20ox-2), Led to the Rice ‘Green Revolution’. Breed Sci 52(2):143–150

    Article  CAS  Google Scholar 

  • Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB, Briggs SP (1995) Cloning and characterization of the maize An1 gene. Plant Cell 7(1):75–84

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14(10):1269–1278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chia N, Guttenberg N (2011) Dynamics of gene duplication and transposons in microbial genomes following a sudden environmental change. Phys Rev E Stat Nonlinear Soft Matter Phys 83(2 Pt 1):021906

    Article  CAS  Google Scholar 

  • Crossa J, Campos GL, Pérez P, Gianola D, Burgueño J, Araus JL, Makumbi D, Singh RP, Dreisigacker S, Yan J (2010) Prediction of genetic values of quantitative traits in plant breeding using pedigree and molecular markers. Genetics 186(2):713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucl Acids Res 38(Web Server issue):W64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan W, Song X, Liu T, Huang Z, Ren J, Hou X, Li Y (2015) Genome-wide analysis of the MADS-box gene family in Brassica rapa (Chinese cabbage). Mol Genet Genome (MGG) 290(1):239–255

    Article  CAS  Google Scholar 

  • Duvick DN, Smith JSC, Cooper M (2004) Long-term selection on a commercial hybrid maize breeding program. Plant Breed Rev 24:109–151

    Google Scholar 

  • Fernandez MGS, Becraft PW, Yin Y, Lcobberstedt T (2009) From dwarves to giants? plant height manipulation for biomass yield. Trends Plant Sci 14(8):454

    Article  CAS  Google Scholar 

  • Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ (2010) Phytochrome regulation of branching in Arabidopsis. Plant Physiol 152(4):1914–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Mistry J, Schusterböckler B, Griffithsjones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R (2006) Pfam: clans, web tools and services. Nucl Acids Res 34(Database issue):247–251

    Article  CAS  Google Scholar 

  • Furey A, Harvey I (2011) Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol 157(3):1128

    Article  CAS  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucl Acids Res 31(13):3784–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grassi L, Fusco D, Sellerio A, Corà D, Bassetti B, Caselle M, Lagomarsino MC (2010) Identity and divergence of protein domain architectures after the yeast whole-genome duplication event. Mol BioSyst 6(11):2305–2315

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Rupe MA, Dieter JA, Zou J, Spielbauer D, Duncan KE, Howard RJ, Hou Z, Simmons CR (2010) Cell number regulator 1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 22(4):1057–1073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao QN, Xin AZ, Ai HS, Cheng W, Rong Z, Shui LC (2011) Identification of genes associated with nitrogen-use efficiency by genome-wide transcriptional analysis of two soybean genotypes. BMC Genom 12(1):525

    Article  CAS  Google Scholar 

  • Hartwig T, Chuck GS, Fujioka S, Klempien A, Weizbauer R, Potluri DP, Choe S, Johal GS, Schulz B (2011) Brassinosteroid control of sex determination in maize. Proc Natl Acad Sci USA 108(49):19814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedden P (2003) The genes of the green revolution. Trends Genet 19(1):5–9

    Article  CAS  PubMed  Google Scholar 

  • Hill WG (2010) Understanding and using quantitative genetic variation. Philos Trans R Soc Lond 365(1537):73–85

    Article  Google Scholar 

  • Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai WC, Hanada A, Alonso JM, Ecker JR (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20(2):320–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes TE, Langdale JA, Kelly S (2014) The impact of widespread regulatory neofunctionalization on homeolog gene evolution following whole-genome duplication in maize. Genome Res 24(8):1348–1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kogelman LJA, Keren B, Tony V, Watson-Haigh NS, Kadarmideen HN, Kijas JW, Oddy HV, Gardner GE, Cedric G, Tellam RL (2011) Genetic architecture of gene expression in ovine skeletal muscle. BMC Genom 12(1):607

    Article  CAS  Google Scholar 

  • Lawit SJ, Wych HM, Xu D, Kundu S, Tomes DT (2010) Maize DELLA proteins dwarf plant8 and dwarf plant9 as modulators of plant development. Plant Cell Physiol 51(11):1854

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Cheng Y, Jin J, Jin X, Jiang H, Yan H, Cheng B (2014) Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes. PLoS ONE 9(7):e102825

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu J, Peatman E, Tang H, Lewis J, Liu Z (2012) Profiling of gene duplication patterns of sequenced teleost genomes: evidence for rapid lineage-specific genome expansion mediated by recent tandem duplications. BMC Genom 13(1):246

    Article  CAS  Google Scholar 

  • Magome H, Nomura T, Hanada A, Takedakamiya N, Ohnishi T, Shinma Y, Katsumata T, Kawaide H, Kamiya Y, Yamaguchi S (2013) CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc Natl Acad Sci USA 110(5):1947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16(4):510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masuko H, Endo M, Saito H, Hakozaki H, Park JI, Kawagishi-Kobayashi M, Takada Y, Okabe T, Kamada M, Takahashi H (2006) Anther-specific genes, which expressed through microsporogenesis, are temporally and spatially regulated in model legume, Lotus japonicus. Genes Genet Syst 81(1):57–62

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100(26):15682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morioka K, Yockteng R, Almeida AMR, Specht CD (2015) Loss of YABBY2-like gene expression may underlie the evolution of the laminar style in canna and contribute to floral morphological diversity in the Zingiberales. Front Plant Sci 6:1106

    Article  PubMed  PubMed Central  Google Scholar 

  • Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS (2003) Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302(5642):81

    Article  CAS  PubMed  Google Scholar 

  • Onishi M, Yasunaga T, Tanaka H, Nishimune Y, Nozaki M (2004) Gene structure and evolution of testicular haploid germ cell-specific genes, Oxct2a and Oxct2b. Genomics 83(4):647–657

    Article  CAS  PubMed  Google Scholar 

  • Peiffer JA, Romay MC, Gore MA, Flintgarcia SA, Zhang Z, Millard MJ, Gardner CAC, Mcmullen MD, Holland JB, Bradbury PJ (2014) The genetic architecture of maize height. Genetics 196(4):1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quraishi UM, Abrouk M, Murat F, Pont C, Foucrier S, Desmaizieres G, Confolent C, Rivière N, Charmet G, Paux E (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J Cell Mol Biol 65(5):745–756

    Article  CAS  Google Scholar 

  • Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol 537(537):337

    Article  CAS  PubMed  Google Scholar 

  • Ruggieri V, Bostan H, Barone A, Frusciante L, Chiusano ML (2016) Integrated bioinformatics to decipher the ascorbic acid metabolic network in tomato. Plant Mol Biol 91(4–5):397

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, De LN, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J Cell Mol Biol 66(4):553

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchishinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6(5):410

    Article  CAS  PubMed  Google Scholar 

  • Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucl Acids Res 34(Web Server issue):W609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Teng W, Yan J, Ma X, Meng Y, Dai J, Li JS (2007) Genetic dissection of plant height by molecular markers using a population of recombinant inbred lines in maize. Euphytica 155(1–2):117–124

    CAS  Google Scholar 

  • Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18(12):1944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Cell Mol Biol 73(3):405

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31(1):46–53

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59(59):253

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Deng D, Shi Y, Miao N, Bian Y, Yin Z (2012a) Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Mol Biol Rep 39(3):2401

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee T, Jin H, Marler B, Guo H (2012b) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucl Acids Res 40(7):e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang Q, Zhao Y, Han G, Zhu S (2015) Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response. Gene 566(1):95–108

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Zhao J, Lu W, Deng D (2017) Gibberellin in plant height control: old player, new story. Plant Cell Rep 36(3):391–398

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xue DQ, Chen XL, Zhang H, Chai XF, Jiang JB, Xu XY, Li JF (2016) Transcriptome analysis of the Cf-12-mediated resistance response to cladosporium fulvum in tomato. Front Plant Sci 7:2012

    Article  PubMed  Google Scholar 

  • Yang T-J (2006) Sequence-Level Analysis of the Diploidization Process in the Triplicated FLOWERING LOCUS C Region of Brassica rapa. Plant Cell Online 18:1339–1347. https://doi.org/10.1105/tpc.105.040535

    Article  CAS  Google Scholar 

  • Yang J, Benyamin B, Mcevoy BP, Gordon S, Henders AK, Nyholt DR, Madden PA, Heath AC, Martin NG, Montgomery GW (2010) Common SNPs explain a large proportion of the heritability for human height. Nat Genet 42(7):565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan JS, Tiller KH, Alahmad H, Stewart NR, Stewart CN (2008) Plants to power: bioenergy to fuel the future. Trends Plant Sci 13(8):421

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, Huang Q, Guo X, Dong Z, Wang H (2010) Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Mol Biol 72(4–5):407–421

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Wu J, Zheng Q, Jiang Y, Zhang M, Zhu S (2017) Genome-wide identification and comparative analysis of Alfin-like transcription factors in maize. Genes Genom 39(3):261–275

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by Grants from the National Natural Science Foundation of China (91435110, 31540042, 31701436) and the National Program on Key Basic Research Project (973 Program, No. 2014CB138204). We are grateful to Professor Beijiu Cheng for his helpful discussions and dedicated technical assistance.

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Authors and Affiliations

  1. National Engineering Laboratory of Crop Stress Resistance Breeding, Anhui Agricultural University, Hefei, 230036, China

    Hengsheng Wang, Xingen Zhang, Fangxiu Hu, Mingli Liu, Yang Zhao, Yan Wang, Longjiang Gu & Qing Ma

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  1. Hengsheng Wang
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  2. Xingen Zhang
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  3. Fangxiu Hu
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  4. Mingli Liu
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Contributions

Longjiang Gu and Yang Zhao designed the research, collected the samples, and wrote the paper; Hengsheng Wang, Xingen Zhang and Mingli Liu, performed the experiments, analyzed the data, and drafted the manuscript; Fangxiu Hu and Yan Wang designed qRT-PCR primers and finished the qRT-PCR experiment, Qing Ma provided some constructive suggestions to clarify the questions raised by the reviewers and also made careful modifications on the original manuscript. All authors have read and approved the final manuscript.

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Correspondence to Longjiang Gu or Qing Ma.

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The data generated in this study have been deposited in the NCBI Gene Expression Omnibus database (https://www.ncbi.nlm.nih.gov/geo) and are accessible through accession number GSE116366.

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Fig. S1

Distribution of Ka and Ks values of collinear genes among species. (a), (b), (c), and (h) represent the collinear genes of maize and Arabidopsis thaliana, maize and maize, maize and Sorghum bicolor, and maize and rice, respectively. (d), (e), and (g) represent the collinear genes of rice and A. thaliana, rice and rice, and rice and S. bicolor. (f) and (i) represent the collinear genes of A. thaliana and S. bicolor, and A. thaliana and A. thaliana. Collinear gene pairs with a Ka/Ks ratio > 1 are above the black line, and pairs with a Ka/Ks ratio of 0.5–1 are between the black and dotted lines (TIF) (TIFF 6024 kb)

Fig. S2

Steroid biosynthesis pathway, which is related to brassinosteroid biosynthesis (TIF) (TIFF 8775 kb)

Fig. S3

Carotenoid biosynthesis pathway, which is related to abscisic acid and strigolactone syntheses (TIF) (TIFF 10539 kb)

Fig. S4

Diterpenoid biosynthesis pathway, which is related to gibberellin biosynthesis (TIF) (TIFF 7229 kb)

Fig. S5

RNA-seq results for two maize inbred lines and effects of a GA treatment of ‘Chuan29’ (TIF) (TIFF 6672 kb)

Table S1

Sources of all plant height-related genes (XLSX 42 kb)

Table S2

Collinear pairs of plant height-related genes among four species (XLSX 47 kb)

Table S3

Genetic information for the plant height-related genes in maize (XLSX 32 kb)

Table S4

Microsyntenic pairs of plant height-related genes in maize (XLSX 12 kb)

Table S5

Gene ontology (GO) annotation of plant height-related genes (XLSX 12 kb)

Table S6

KEGG annotation of maize genes (P-value < 0.05) (XLSX 10 kb)

Table S7

Original expression profiles of maize plant height-related genes during different developmental stages (XLSX 55 kb)

Table S8

Differential expression of plant height-related genes in maize based on an RNA-seq analysis of tall and dwarf inbred lines (XLSX 40 kb)

Table S9

Distribution of KEGG pathways for the upregulated DEGs (P-value < 0.05) (XLSX 15 kb)

Table S10

Primers used for the quantitative real-time PCR analysis (XLSX 13 kb)

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Wang, H., Zhang, X., Hu, F. et al. Systematic identification and characterization of candidate genes for the regulation of plant height in maize. Euphytica 215, 27 (2019). https://doi.org/10.1007/s10681-019-2345-1

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