Skip to main content
Log in

Gene Expression Analysis in Sorghum Hybrids and Their Parental Lines at Critical Developmental Stages in Relation to Grain Yield Heterosis by Exploiting Heterosis-Related Genes from Major Cereals

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Relative expression levels of selected genes from the Heterosis-Related Gene Database exhibiting more than 90% homology with sorghum were studied in hybrids and their respective parental lines for a better understanding on the molecular basis of heterosis. A high (27A × RS 673) and a low heterotic hybrid (7A × CB 26) of sorghum along with their parental lines were used for this purpose. Twenty (15 maize and 5 rice) genes exhibiting more than 90% homology with that of sorghum were identified. The maize genes ZmHG13, ZmHG16, and ZmhG19 exhibited more than fourfold increase over the male parent (RS 673) of high heterotic hybrid during booting stage, which started decreasing during flowering stage. Similarly, the rice genes OsHG1 and OsHG12 recorded > 2.5-fold increase. However, these genes recorded less than twofold increase during the same stage of the plant in the low heterotic hybrid. Notably, among the genes that exhibited higher expression in the highly heterotic hybrid were those coding for proteins, which were known to play crucial roles in the manifestation of heterosis in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alam MF, Khan MR, Nuruzzaman M, Parvez S, Swaraz AM, Alam I, Ahsan N (2004) Genetic basis of heterosis and inbreeding depression in rice (Oryza sativa L). J Zhejiang Univ SCI 5(4):406–411

    Article  PubMed  CAS  Google Scholar 

  • Bao JY, Lee S, Chen C, Zhang XQ, Zhang Y, Liu SQ, Clark T, Wang J, Cao ML, Yang HM, Wang SM, Yu J (2005) Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol 138:1216–1231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baranwal VK, Venugopal M, Barwale UZ, Tyagi AK, Kapoor S (2012) Heterosis: emerging ideas about hybrid vigour. J Exp Bot 63(18):6309–6314

    Article  PubMed  CAS  Google Scholar 

  • Bassene JB, Froelicher Y, Dubois C, Ferrer RM, Navarro L, Ollitrault P, Ancillo G (2010) Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm. Heredity 105:299–308

    Article  PubMed  CAS  Google Scholar 

  • Ben-Israel I, Kilian B, Nida H, Fridman E (2012) Heterotic trait locus (HTL) mapping identifies intra-locus interactions that underlie reproductive hybrid vigor in Sorghum bicolor. PLoS One 7:e38993

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Birchler JA (2013) Genetic rules of heterosis in plants. In: Chen ZJ, Birchler JA (eds) Polyploid and hybrid genomics. John Wiley & Sons, Inc., Hoboken, pp 313–321

    Chapter  Google Scholar 

  • Blum A (1970) Nature of heterosis in grain production by the sorghum panicle. Crop Sci 10:28–31

    Article  Google Scholar 

  • Blum A (1977) The basis of heterosis in the differentiating sorghum panicle. Crop Sci 17:880–882

    Article  Google Scholar 

  • Conner AB, Karper RE (1927) Hybrid vigor in sorghum. In: Texas Agricultural Experimental Station Bulletin 359. Texas A & M University, College Station

    Google Scholar 

  • Dahan J, Mireau H (2013) The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol 10(9):1469–1476

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eastin JD (1972) Photosynthesis and translocation in relation to plant development. In: Rao NGP, House LR (eds) Sorghum in seventies. Oxford and IBH Publishing Co., New Delhi, pp 214–246

    Google Scholar 

  • Elwafa AA, Ahmed TA, Hassaballa EA, Sayed MA (2005) Heterosis and line × tester analysis of combining ability in grain sorghum [Sorghum bicolor (L.) Moench]. Assiut J Agric Sci 36(1):159–175

    Google Scholar 

  • 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 U S A 109:7109–7114

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaut BS, Clark LG, Wendel JF, Muse SV (1997) Comparisons of the molecular evolutionary process at rbcL and ndhF in the grass family (Poaceae). Mol Biol Evol 14(7):769–777

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845

    Article  PubMed  CAS  Google Scholar 

  • Han P, Lu X, Mi F, Dong J, Xue C, Li J, Han B, Zhang X (2015) Proteomic analysis of heterosis in the leaves of sorghum - sudangrass hybrids. Acta Biochim Biophys Sin 48(2):161–173

    Article  CAS  Google Scholar 

  • Haussmann BI, Obilana AB, Ayiecho PO, Blum AA, Schipprack W, Geiger HH (2000) Yield and yield stability of four population types of grain sorghum in a semi-arid area of Kenya. Crop Sci 40:319–329

    Google Scholar 

  • He GM, Zhu XP, Elling AA, Chen LB, Wang XF, Guo L, Liang MZ, He H, Zhang HY, Chen FF, Qi Y, Chen R, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hemlata S, Vithal S (2006) Heterosis in Sorghum (Sorghum bicolor L. Moench). Agr Sci Digest 26(4):245–248

    Google Scholar 

  • Hochholdinger F, Hoeckenger N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432

    Article  PubMed  CAS  Google Scholar 

  • Hovny MRA (2000) Heterosis and combining ability in grain sorghum [Sorghum bicolor (L.) Moench]. Assiut J Agric Sci 31(3):17–30

    Google Scholar 

  • Jain SK, Patel PR (2013) Heterosis studies for yield and its attributing traits in sorghum [Sorghum bicolor (L.) Moench]. Forage Res 39(3):114–117

    Google Scholar 

  • Klein RR, Mullet JE, Jordan DR, Miller FR, Rooney WL, Menz MM, Franks CD, Klein PE (2008) The effect of tropical sorghum conversion and inbred development on genome diversity as revealed by high-resolution genotyping. Crop Sci 48(S1):S12–S26

    Google Scholar 

  • Lamkey KR, Edwards JW (1999) The quantitative genetics of heterosis. In: Coors JG, Pandey S (eds) Proceedings of the International Symposium on the Genetics and Exploitation of Heterosis in Crops, CIMMYT, Mexico City, Mexico, 17–22 Aug. 1997. ASA, CSSA, and SSSA, Madison, pp 31–48

    Google Scholar 

  • Li C, Huang L, Xu C, Zhao Y, Zhou DX (2011) Altered levels of histone deacetylase OsHDT1 affect differential gene expression patterns in hybrid rice. PLoS One 6:e21789

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66

    Article  PubMed  CAS  Google Scholar 

  • Lu XP, Liu DD, Wang SY, Mi FG, Han PA, Lu ES (2014) Genetic effects and heterosis prediction model of Sorghum bicolor × S. sudanense grass. Acta Agron Sin 40(3):466–475

    Article  CAS  Google Scholar 

  • Meyer S, Pospisil H, Scholten S (2007) Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol Biol 63:381–391

    Article  PubMed  CAS  Google Scholar 

  • Meyer RC, Witucka-Wall H, Becher M, Blacha A, Boudichevskaia A, Dörmann P, Fiehn O, Friedel S, von Korff M, Lisec J, Melzer M, Repsilber D, Schmidt R, Scholz M, Selbig J, Willmitzer L, Altmann T (2012) Heterosis manifestation during early Arabidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids. Plant J 71:669–683

    Article  PubMed  CAS  Google Scholar 

  • Miller FR, Kebede Y (1984) Genetic contributions to yield gains in sorghum: 1950 to 1980. In: Fehr WR (ed) Genetic contributions to yield gains of five major crop plants, vol 7. Crop Science Society of America, Madison, pp 1–14

    Google Scholar 

  • Nagaraja Reddy R, Madhusudhana R, Murali Mohan S, Chakravarthi DV, Mehtre SP, Seetharama N, Patil JV (2013) Mapping QTL for grain yield and other agronomic traits in post-rainy sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 126:1921–1939

    Article  PubMed  CAS  Google Scholar 

  • Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  PubMed  CAS  Google Scholar 

  • Nie HS, Li SP, Shan XH, Wu Y, Su SZ, Liu HK, Han JY, Yuan YP (2015) Analysis of gene expression patterns and levels in maize hybrids and their parents. Genet Mol Res 14(4):15399–15411

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101(26):9903–9908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  PubMed  CAS  Google Scholar 

  • Pea G, Ferron S, Gianfranceschi L, Krajewski P, Pe ME (2008) Gene expression non-additivity in immature ears of a heterotic F1 maize hybrid. Plant Sci 174:17–24

    Article  CAS  Google Scholar 

  • Quinby JR (1974) Sorghum improvement and the genetics of growth. Texas A & M Univ. Press, College Station

    Google Scholar 

  • Ringo J, Onkware A, Mgonja M, Deshpande S, Rathore A, Mneney E, Gudu S (2015) Heterosis for yield and its components in sorghum (Sorghum bicolor L. Moench) hybrids in dry lands and sub-humid environments of East Africa. Aust J Crop Sci 9(1):9–13

    CAS  Google Scholar 

  • Saeki N, Kawanabe T, Ying H, Shimizu M, Kojima M, Abe H, Okazaki K, Kaji M, Taylor JM, Sakakibara H, Peacock WJ, Dennis ES, Fujimoto R (2016) Molecular and cellular characteristics of hybrid vigour in a commercial hybrid of Chinese cabbage. BMC Plant Biol 16:45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Shafi W, Haribhushan A, Singh NB (2011) The magic of heterosis: new tools and complexities. Nat Sci 9:42–53

    Google Scholar 

  • Seifert GJ (2004) Nucleotide sugar inter-conversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7:277–284

    Article  PubMed  CAS  Google Scholar 

  • Smith CW, Frederiksen RA (2000) Sorghum—origin, history, technology and production. John Wiley & Sons, Inc, New York

    Google Scholar 

  • Song S, Huang Y, Wang X, Wei G, Qu H, Wang W, Ge X, Hu S, Liu G, Liang Y, Yu J (2009) HRGD: a database for mining potential heterosis-related genes in plants. Plant Mol Biol 69:255–260

    Article  PubMed  CAS  Google Scholar 

  • Song GS, Zhai HL, Peng YG, Zhang L, Wei G, Chen XY, Xiao YG, Wang L, Chen YJ, Wu B, Chen B, Zhang Y, Chen H, Feng XJ, Gong WK, Liu Y, Yin ZJ, Wang F, Liu GZ, Xu HL, Wei XL, Zhao XL, Ouwerkerk PB, Hankemeier T, Reijmers T, van der Heijden R, Lu CM, Wang M, van der Greef J, Zhu Z (2010) Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol Plant 3:1012–1025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srinivas G, Satish K, Madhusudhana R, Nagaraja Reddy R, Murali Mohan S, Seetharama N (2009) Identification of quantitative trait loci for agronomically important traits and their association with genic-microsatellite markers in sorghum. Theor Appl Genet 118:1439–1454

    Article  PubMed  CAS  Google Scholar 

  • Stephens JC, Holland RF (1954) Cytoplasmic male sterility for hybrid sorghum seed production. Agron J 46:20–23

    Article  Google Scholar 

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci U S A 103(18):6801–6810

    Article  CAS  Google Scholar 

  • Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14(10):1916–1923

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thiemann A, Fu J, Schrag TA, Melchinger AE, Frisch M, Scholten S (2010) Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L. Theor Appl Genet 120:401–413

    Article  PubMed  CAS  Google Scholar 

  • Thiemann A, Fu J, Seifert F, Grant-Downton RT, Schrag TA, Pospisil H, Frisch M, Melchinger AE, Scholten S (2014) Genome-wide meta-analysis of maize heterosis reveals the potential role of additive gene expression at pericentromeric loci. BMC Plant Biol 14:88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vanderlip RL, Reeves HE (1972) Growth stages of sorghum. Agron J 64:13–16

    Article  Google Scholar 

  • Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, Li X, Song G, Zhai H, Peng Y, Li D, Xu H, Wei X, Cao M, Deng H, Xin Y, Fu X, Yuan L, Yu J, Zhu Z, Zhu L (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci U S A 106:7695–7701

    Article  PubMed  PubMed Central  Google Scholar 

  • Willems E, Leyns L, Vandesompele J (2008) Standardization of real-time PCR gene expression data from independent biological replicates. Anal Biochem 379:127–129

    Article  PubMed  CAS  Google Scholar 

  • Zhang HY, He H, Chen LB, Li L, Liang MZ, Wang XF, Liu XG, He GM, Chen RS, Ma LG, Deng XW (2008) A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant 1(5):720–731

    Article  PubMed  CAS  Google Scholar 

  • Zhang XM, Xiao N, Zhang HX, Feng YX, Liu ZX, Gao Y, Dai ZY, Chen JM (2012) Analysis of the relationship between differential expression of rice gene and heterosis. China Agric Sci 45(7):1235–1245

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Director of ICAR – Indian Institute of Millets Research, Hyderabad, for providing the facilities. IJ thanks the Osmania University, Hyderabad for permitting him to register for Ph.D. to complete his dissertation work.

Funding

This study was funded by the grant received from Department of Biotechnology, Government of India, under Rapid Grant for Young Investigators (Grant No. BT/PR/13256/GBD/27/240/2009).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Passoupathy Rajendrakumar.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic Supplementary Material

ESM 1

(PDF 343 kb)

ESM 2

(PDF 417 kb)

ESM 3

(PDF 56 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaikishan, I., Rajendrakumar, P., Hariprasanna, K. et al. Gene Expression Analysis in Sorghum Hybrids and Their Parental Lines at Critical Developmental Stages in Relation to Grain Yield Heterosis by Exploiting Heterosis-Related Genes from Major Cereals. Plant Mol Biol Rep 36, 418–428 (2018). https://doi.org/10.1007/s11105-018-1079-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-018-1079-x

Keywords

Navigation