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Journal of Integrative Agriculture  2016, Vol. 15 Issue (12): 2726-2735    DOI: 10.1016/S2095-3119(16)61376-X
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Heterotic loci identified for plant height and ear height using two CSSLs test populations in maize
WANG Hong-qiu1, 2*, ZHANG Xiang-ge2, 3*, YANG Hui-li2, CHEN Yong-qiang2, YUAN Liang2, LI Wei-hua2, LIU Zong-hua2, TANG Ji-hua2, KANG Ding-ming1
1 College of Agriculture and Biotechnology, China Agricultural University, Beijing 100193, P.R.China
2 National Key Laboratory of Wheat and Maize Crop Science, Ministry of Education/Collaborative Innovation Center of Henan Grain Crops, College of Agronomy, Henan Agricultural University, Zhengzhou 450002, P.R.China
3 College of Agronomy, Sichuan Agricultural University, Chengdu 611130, P.R.China
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Abstract       Heterosis is an important biological phenomenon, and it has been used to increase grain yield, quality and resistance to abiotic and biotic stresses in many crops. However, the genetic mechanism of heterosis remains unclear up to now. In this study, a set of 184 chromosome segment substitution lines (CSSLs) population, which derived from two inbred lines lx9801 (the recurrent parent) and Chang 72 (the donor parent), were used as basal material to construct two test populations with the inbred lines Zheng 58 and Xun 9058. The two test populations were evaluated in two locations over two years, and the heterotic loci for plant height and ear height were identified by comparing the performance of each test hybrid with the corresponding CK at P<0.05 significant level using one-way ANOVA analysis and Duncan’s multiple comparisons. There were 24 and 29 different heterotic loci (HL) identified for plant height and ear height in the two populations at two locations over two years. Three HL (hlPH4a, hlPH7c, hlPH1b) for plant height and three (hlEH1d, hlEH6b, hlEH1b) for ear height were identified in the CSSLs×Zheng 58 and CSSLs×Xun 9058 populations as contributing highly to heterosis performance of plant height and ear height across four environments. Among the 29 HL identified for ear height, 12 HL (41.4%) shared the same chromosomal region associated with the HL (50.0%) identified for plant height in the same test population and environment.
Keywords:  maize        CSSLs test population        plant height        ear height        heterotic loci  
Received: 08 December 2015   Accepted:
Fund: 

This work was supported by the National Basic Research Program of China (2014CB138203) and the National Natural Science Foundation of China (31271732).

Corresponding Authors:  KANG Ding-ming, Tel: +86-10-62732565, Fax: +86-10-62733404, E-mail: kdm@pku.edu.cn; TANG Ji-hua, Tel: +86-371-63558377, Fax: +86-371-63558122, E-mail: tangjihua1@163.com   
About author:  WANG Hong-qiu, E-mail: hqwang@cau.edu.cn;

Cite this article: 

WANG Hong-qiu, ZHANG Xiang-ge, YANG Hui-li, CHEN Yong-qiang, YUAN Liang, LI Wei-hua, LIU Zong-hua, TANG Ji-hua, KANG Ding-ming. 2016. Heterotic loci identified for plant height and ear height using two CSSLs test populations in maize. Journal of Integrative Agriculture, 15(12): 2726-2735.

Austin D F, Lee M, Veldboom L R. 2001. Genetic mapping in maize with hybrid progeny across testers and generations: Plant height and flowering. Theoretical and Applied Genetics, 102, 163–176.

Beavis W D, Grant D, Albertsen M, Fincher R. 1991. Quantitative trait loci for plant height in four maize populations and their associations with qualitative genetic loci. Theoretical and Applied Genetics, 83,141–145.

Bruce A B. 1910. The Mendelian theory of heredity and the augmentation of vigor. Science, 32, 627–628.

Chen Z J. 2013. Genomic and epigenetic insights into the molecular bases of heterosis. Nature Reviews Genetics, 14, 471–482.

East E M. 1936. Heterosis. Genetics, 21, 375–397.

Dahal D, Mooney B P, Newton K J. 2012. Specific changes in total and mitochondrial proteomes are associated with higher levels of heterosis in maize hybrids. The Plant Journal, 72, 70–83.

Fievet J B, Dillmann C, de Vienne D. 2010. Systemic properties of metabolic networks lead to an epistasis-based model for heterosis. Theoretical and Applied Genetics, 120, 463–473.

Frascaroli E, Canè M A, Landi P, Pea G, Gianfranceschi L, Villa M, Morgante M, Pè M E. 2007. Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics, 176, 625–644.

Fujimoto R, Taylor J M, Shirasawa S, Peacock W J, Dennis E S. 2012. Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proceedings of the National Academy of Sciences of the United States of America, 109, 7109–7114.

Guo M, Rupe M A, Yang X F, Crasta O, Zinselmeier C, Smith O S, Bowen B. 2006. Genome-wide transcript analysis of maize hybrids: Allelic additive gene expression and yield heterosis. Theoretical and Applied Genetics, 113, 831–845.

Guo X, Guo Y P, Ma J, Wang F, Sun M Z, Gui L J, Zhou J J, Song X L, Sun X Z, Zhang T Z. 2013. Mapping heterotic loci for yield and agronomic traits using chromosome segment introgression lines in cotton. Journal of Integrative Plant Biology, 55, 759–774.

Hua J, Xing Y, Wu W, Xu C, Sun X, Yu S, Zhang Q. 2003. Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid.  Proceedings of the National Academy of Sciences of the United States of America, 100, 2574–2579.

Jones D F. 1917. Dominance of linked factors as a means of accounting for heterosis. Genetics, 2, 466–479.

Koester R, Sisco P H, Stuber C W. 1993. Identification of quantitative trait loci controlling days to flowering and plant height in two near isogenic lines of maize. Crop Science, 33, 1209–1216.

Kusterer B, Piepho H P, Utz H F, Schön C C, Muminovic J, Meyer R C, Altmann T, Melchinger A E. 2007. Heterosis for biomass-related traits in Arabidopsis investigated by quantitative trait loci analysis of the triple testcross design with recombinant inbred lines. Genetics, 177, 1839–1850.

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: multi parental quantitative trait loci mapping reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.). Genetics, 190, 795–811.

Li L Z, Lu K Y, Chen Z M, Mou T M, Hu Z L, Li X Q. 2008. Dominance, overdominance and epistasis condition the heterosis in two heterotic rice hybrids. Genetics, 180, 1725–1742.

Li Y C, Peng J H, Liu Z Q. 1997. Heterosis and combining ability for plant height and its components in hybrid wheat with Triticum timopheevi cytoplasm. Euphytica, 95, 337–345.

Li Z K, Luo L J, Mei H W, Wang D L, Shu Q Y, Tabien R, Zhong D B, Ying C S, Stansel J W, Khush G S, Paterson A H. 2001. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics, 158, 1737–1753.

Li Z K, Xie Q G, Zhu Z L, Liu J L, Han S X, Tian B, Yuan Q Q, Tian J C. 2010.  Analysis of plant height heterosis based on QTL mapping in wheat. Acta Agronomic Sinica, 36, 771–778. (in Chinese)

Lippman Z, Zamir D. 2007. Heterosis: Revisiting the magic. Trends in Genetics, 23, 60–66.

Liu G F, Zhu H T, Zhang G Q, Li L H, Ye G Y. 2012. Dynamic analysis of QTLs on tiller number in rice (Oryza sativa L.) with single segment substitution lines. Theoretical and Applied Genetics, 125, 143–153.

Luo L J, Li Z K, Mei H W, Shu Q Y, Tabien R, Zhong D B, Ying C S, Stansel J W, Khush G S, Paterson A H. 2001. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. Genetics, 158, 1755–1771.

Luo X J, Fu Y C, Zhang P J, Wu S, Tian F, Liu J Y, Zhu Z F, Yang J S, Sun C Q. 2009. Additive and overdominant effects resulting from epistatic loci are the primary genetic basis of heterosis in rice. Journal Integrative Plant Biology, 51, 393–408.

Ma L Y, Bao J S, Guo L B, Zeng D L, Li X M, Ji Z J, Xia Y W, Yang C D, Qian Q. 2009. Quantitative trait loci for panicle layer uniformity identified in doubled haploid lines of rice in two environments. Journal Integrative Plant Biology, 51, 818–824.

Melchinger A E, Utz H F, Schön C C. 1998. Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics, 149, 383–403.

Meyer R C, Kusterer B, Lisec J, Steinfath M, Becher M, Scharr H, Melchinger A E, Selbig J, Schurr U, Willmitzer L, Altmann T. 2010. QTL analysis of early stage heterosis for biomass in Arabidopsis. Theoretical and Applied Genetics, 120, 227–237.

Pikaard C S. 2000. The epigenetics of nucleolar dominance. Trends in Genetics, 16, 495–500.

Powers L. 1944. An expansion of Jones’s theory for the explanation of heterosis. American Naturalist, 78, 275.

Qu Z, Li L, Luo J, Wang P, Yu S, Mou T, Zheng X, Hu Z. 2012. QTL mapping of combining ability and heterosis of agronomic traits in rice backcross recombinant inbred lines and hybrid crosses. PLOS ONE, 7, e28463.

Radoev M, Becker H C, Ecke W. 2008. Genetic analysis of heterosis for yield and yield components in rapeseed (Brassica napus L.) by quantitative trait locus mapping. Genetics, 179, 1547–1558.

Riedelsheimer C, Czedik-Eysenberg A, Grieder C, Lisec J, Technow F, Sulpice R, Altmann T, Stitt M, Willmitzer L, Melchingerothar A E. 2012. Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nature Genetics, 44, 217–220.

Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger A E. 2012. Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proceedings of the National Academy of Sciences of the United States of America, 109, 8872–8877.

Schön C C, Dhillon B S, Utz H F, Melchinger A E. 2010. High congruency of QTL positions for heterosis of grain yield in three crosses of maize. Theoretical and Applied Genetics, 120, 321–332.

Schnable P S, Springer N M. 2013. Progress toward understanding heterosis in crop plants. Annual Review of Plant Biology, 64, 71–78.

Semel Y, Nissenbaum J, Menda N, Zinder M, Krieger U, Issman N, Pleban T, Lippman Z, Gur A, Zamir D. 2006. Overdominant quantitative trait locus for yield and fitness in tomato.  Proceedings of the National Academy of Sciences of the United States of America, 103, 12981–12986.

Shen G J, Zhan W, Chen H X, Xing Y Z. 2014. Dominance and epistasis are the main contributors to heterosis for plant height in rice. Plant Science, 215–216, 11–18.

Shull G H. 1908. The composition of a field of maize. Journal of Heredity, 1, 296–301.

Song F W, Peng H R, Liu T, Zhang Y R, Sun Q X, Ni Z F. 2011. Heterosis for plant height and ear position in maize revealed by quantitative trait loci analysis with triple testcross design. Acta Agronomica Sinica, 37, 1186–1195. (in Chinese)

Sun Q, Li W C, Zhang F J, Yu Y L, Zhang Q W, Dou S Q, Meng Z D. 2014. Analysis on the pedigree of the parental lines of the maize hybrids approved by the nation from 2001 to 2012. Journal of Maize Sciences, 22, 6–11, 15. (in Chinese)

Syed N H, Chen Z J. 2005. Molecular marker genotypes, heterozygosity and genetic interactions explain heterosis in Arabidopsis thaliana. Heredity, 94, 295–304.

Tang J H, Ma X Q, Teng W T, Yan J B, Wu W R, Dai J R, Li J S. 2006. Detection of heterotic locus and quantitative trait loci for plant height using an immortalized F2 population in maize. Chinese Science Bulletin, 51, 2864–2869.

Tang J H, Yan J B, Ma X Q, Teng W T, Wu W R, Dai J R, Dhillon B S, Melchinger A E, Li J S. 2010. Dissection of the genetic basis of heterosis in an elite maize hybrid by QTL mapping in an immortalized F2 population. Theoretical and Applied Genetics, 120, 333–340.

Tang Z X, Yang Z F, Hu Z Q, Zhang D, Lu X, Jia B, Deng D X, Xu C W. 2013.  Cytonuclear epistatic quantitative trait locus mapping for plant height and ear height in maize. Molecular Breeding, 3, 11–14.

Veldboom L R, Lee M. 1996. Genetic mapping of quantitative trait loci in maize in stress and nonstress environments. II. Plant height and flowering. Crop Science, 36, 1320–1327.

Wang J K, Wan X Y, Crossa J, Crouch J, Weng J F, Zhai H Q, Wan J M. 2006. QTL mapping of grain length in rice (Oryza sativa L.) using chromosome segment substitution lines. Genetisc Research, 88, 93–104.

Wang Y, Yao J, Zhang Z F, Zheng Y L. 2006. The comparative analysis based on maize integrated QTL map and meta-analysis of plant height QTLs. Chinese Science Bulletin, 51, 2219–2230.

Wang Z, Ni Z, Wu H, Nie X, Sun Q. 2006. Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 113, 1283–1294.

Wang Z Q, Yu C Y, Liu X, Liu S J, Yin C B, Liu L L, Lei J G, Jiang L, Yang C, Chen L M, Zhai H Q, Wan J M. 2012. Identification of indica rice chromosome segments for the improvement of japonica inbreds and hybrids. Theoretical and Applied Genetics, 124, 1351–1364.

Wei X Y, Wang B, Peng Q, Wei F, Mao K J, Zhang X G, Sun P, Liu Z H, Tang J H. 2015. Heterotic loci for various morphological traits of maize detected using a single segment substitution lines test-cross population. Molecular Breeding, 35, 94.

Williams W. 1959. Heterosis and the genetics of complex characters. Nature, 184, 527–530.

Xiao J, Li J, Yuan L, Tanksley S D. 1995. Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genetics, 140, 45–54.

Yan J B, Tang H, Huang Y Q, Zheng Y L, Li J S. 2003. Dynamic QTL analysis for plant height in different developing stages in maize. Chinese Science Bulletin, 48, 1959–1964.

Yu C Y, Wan J M, Zhai H Q, Wang C M, Jiang L, Xiao Y H, Liu Y Q. 2005. Study on heterosis of inter-subspecies between indica and japonica rice (Oryza sativa L.) using chromosome segment substitution lines. Chinese Science Bulletin, 50, 131–136.

Yu S B, Li J X, Xu C G, Tan Y F, Gao Y J, Li X H, Zhang Q F, Saghai Maroof M A. 1997. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proceedings of the National Academy of Sciences of the United States of America, 94, 9226–9231.

Yu S B, Li J X, Xu C G, Tan Y F, Li X H, Zhang Q F. 2002. Identification of quantitative trait loci and epistatic interactions for plant height and heading date in rice. Theoretical and Applied Genetics, 104, 619–625.

Yuan L, Ding D, Li W H, Xie H L, Tang J H, Fu Z Y. 2012. Construction of single segment substitution lines (SSSLs) of the elite inbred lines in maize. Journal of Maize Sciences, 20, 52–55. (in Chinese)

Zhang K P, Tian J C, Zhao L, Wang S S. 2008. Mapping QTLs with epistatic effects and QTL×environment interactions for plant height using a doubled haploid population in cultivated wheat. Journal of Genetics and Genomics, 35, 119–127.

Zhang Y, Li Y X, Wang Y, Liu Z Z, Liu C, Peng B, Tan W W, Wang D, Shi Y S, Sun B C, Song Y C, Wang T Y, Li Y. 2010. Stability of QTL across environments and QTL-by-environment interactions for plant and ear height in maize. Agricultural Sciences in China, 9, 1400–1412.

Zhang Y, Ni Z F, Yao Y Y, Nie X L, Sun Q X. 2007. Gibberellins and heterosis of plant height in wheat (Triticum aestivum L.). BMC Genetics, 8, 1471–2156.

Zhou G, Chen Y, Yao W, Zhang C J, Xie W B, Hua J P, Xing Y Z, Xiao J H, Zhang Q F. 2012. Genetic composition of yield heterosis in an elite rice hybrid. Proceedings of the National Academy of Sciences of the United States of America, 109, 15847–15852.
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