Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (9): 2477-2491    DOI: 10.1016/j.jia.2022.07.006
Special Issue: 玉米遗传育种合辑Maize Genetics · Breeding · Germplasm Resources
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Heterosis and heterotic patterns of maize germplasm revealed by a multiple-hybrid population under well-watered and drought-stressed conditions

SANG Zhi-qin1, 2, 3, ZHANG Zhan-qin2, YANG Yu-xin3, LI Zhi-wei3, LIU Xiao-gang3, XU Yun-bi3, 4, LI Wei-hua1 #br#

1 Key Laboratory of Oasis Eco-Agriculture, Xinjiang Production and Construction Corps/Agricultural College, Shihezi University, Shihezi 832003, P.R.China

2 Xinjiang Academy of Agricultural and Reclamation Science, Shihezi 832000, P.R.China

3 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China

4 International Maize and Wheat Improvement Center (CIMMYT), El Batan Texcoco 56130, Mexico

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

本研究以41个代表性的玉米自交系通过不完全双列杂交产生了737个杂种F1的多杂种群体(MPH),将MPH群体分别种植在干旱和正常滴水处理下,利用38737个单核苷酸多态性标记(SNPs)对41份亲本进行了全基因组扫描。41份亲本自交系间的遗传距离为0.05到0.74之间,依据遗传距离可以将其划分为5个杂种优势群。根据不同杂种优势群产生杂交种的表型(产量、生育期、株高),研究认为BSSS×NSS、NSS×SPT和BSSS×SPT这3种杂优模式在中国机收玉米育种中具有较大的利用价值。研究一般配合力和特殊配合力的比值表明,正常滴水下加性效应对单株产量的的影响较大,而在干旱处理下非加性效应对产量的影响力更大。干旱条件下高产的玉米杂交种其亲本之一必须是配合力较高或者抗旱性较好的玉米自交系。在一定的遗传距离(GD)范围内,GD和杂种产量和产量杂种优势呈正相关。本研究认为杂种优势是亲本优势基因位点逐步累加和亲本间最佳遗传距离共同作用形成的,干旱处理下的产量杂种优势主要由非加性效应决定的。 




Abstract  Understanding the heterosis in multiple environments between different heterotic groups is of fundamental importance in successful maize breeding.  A total of 737 hybrids derived from 41 maize inbreds were evaluated over two years, with the aim of assessing the genetic diversity and their performance between heterotic groups under drought-stressed (DS) and well-watered (WW) treatments.  A total of 38 737 SNPs were employed to assess the genetic diversity.  The genetic distance (GD) between the parents ranged from 0.05 to 0.74, and the 41 inbreds were classified into five heterotic groups.  According to the hybrid performance (high yield and early maturity between heterotic groups), the heterosis and heterotic patterns of Iowa Stiff Stalk Synthetic (BSSS)×Non-Stiff Stalk (NSS), NSS×Sipingtou (SPT) and BSSS×SPT were identified to be useful options in China’s maize breeding.  The relative importance of general and specific combining abilities (GCA and SCA) suggests the importance of the additive genetic effects for grain yield traits under the WW treatment, but the non-additive effects under the DS treatment.  At least one of the parental lines with drought tolerance and a high GCA effect would be required to achieve the ideal hybrid performance under drought conditions.  GD showed a positive correlation with yield and yield heterosis in within-group hybrids over a certain range of GD.  The present investigation suggests that the heterosis is due to the combined accumulation of superior genes/alleles in parents and the optimal genetic distance between parents, and that yield heterosis under DS treatment was mainly determined by the non-additive effects.
Keywords:  maize        drought stress        heterosis        heterotic group        heterotic pattern        genetic distance  
Received: 26 December 2020   Accepted: 01 April 2021
Fund: This study was supported by the National Natural Science Foundation of China (31760424) and the Scientific and Technological Project of Xinjiang Production and Construction Corps of China (2019AB021).  
About author:  SANG Zhi-qin, E-mail: sangzhiqin@126.com; Correspondence LI Wei-hua, Mobile: +86-18997736665, E-mail: lwh_agr@shzu.edu.cn; XU Yun-bi, E-mail: y.xu@cgiar.org

Cite this article: 

SANG Zhi-qin, ZHANG Zhan-qin, YANG Yu-xin, LI Zhi-wei, LIU Xiao-gang, XU Yunbi, LI Wei-hua. 2022. Heterosis and heterotic patterns of maize germplasm revealed by a multiple-hybrid population under well-watered and drought-stressed conditions. Journal of Integrative Agriculture, 21(9): 2477-2491.

Adebayo M A, Menkir A, Blay E, Gracen V, Danquah E. 2017. Combining ability and heterosis of elite drought-tolerant maize inbred lines evaluated in diverse environments of lowland tropics. Euphytica, 213, 43.
Ahmad M, Saleem M, Ahsan M, Ahmad A. 2016. Genetic analysis of water-deficit response traits in maize. Genetics and Molecular Research, 15, 15017459. 
Alexander D H, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655–1664. 
Amiruzzaman M, Islam M A, Hassan L, Rohman M. 2010. Combining ability and heterosis for yield and component characters in maize. Academic Journal of Plant Sciences, 3, 79–84. 
Badu-Apraku B, Oyekunle M, Akinwale R O, Aderounmu M. 2013. Combining ability and genetic diversity of extra-early white maize inbreds under stress and nonstress environments. Crop Science, 53, 9–26. 
Balestre M, Machado J C, Lima J L, Souza J C, Nóbrega F. 2008. Genetic distance estimates among single cross hybrids and correlation with specific combining ability and yield in corn double cross hybrids. Genetics and Molecular Research, 7, 65–73. 
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 1406, 133–199.
Betrán F J, Ribaut J M, Beck D, Leon D, De G. 2003. Genetic diversity, specific combining ability, and heterosis in tropical maize under stress and nonstress environments. Crop Science, 43, 797–806. 
Bolaños J, Edmeades G O. 1993. Eight cycles of selection for drought tolerance in lowland tropical maize. II. Responses in reproductive behavior. Field Crops Research, 31, 253–268. 
Bolaños J, Edmeades G O. 1996. The importance of the anthesis-silking interval in breeding for drought tolerance in tropical maize. Field Crops Research, 48, 65–80. 
Campos H, Cooper M, Edmeades G O, Loffler C, Schussler J R, Ibanez M. 2006. Changes in drought tolerance in maize associated with fifty years of breeding for yield in the US corn belt. Maydica, 51, 369–381.
Choukan R, Hossainzadeh A, Ghannadha M R, Warburton M L, Talei A R, Mohammadi S A. 2006. Use of SSR data to determine relationships and potential heterotic groupings within medium to late maturing Iranian maize inbred lines. Field Crops Research, 95, 212–222.
Derera J, Tongoona P, Vivek B S, Laing M D. 2008. Gene action controlling grain yield and secondary traits in southern African maize hybrids under drought and non-drought environments. Euphytica, 162, 411–422. 
Dermail A, Suriharn B, Chankaew S, Sanitchon J, Lertrat K. 2020. Hybrid prediction based on SSR-genetic distance, heterosis and combining ability on agronomic traits and yields in sweet and waxy corn. Scientia Horticulturae, 259, 108817.
Ertiro B T, Semagn K, Das B, Olsen M, Labuschagne M, Worku M, Weganry D, Azmach G, Ogugo V, Abebe B, Chibsa T, Menkir A. 2017. Genetic variation and population structure of maize inbred lines adapted to the mid-altitude sub-humid maize agro-ecology of ethiopia using single nucleotide polymorphic (SNP) markers. BMC Genomics, 18, 777.
FAO (Food and Agriculture Organization). 2019. Online statistical database: food balance. FAOSTAT. [2019-07-03] http://www.fao.org/faost at/en/#data.
Griffing B. 1956. Concept of general and specific combining ability in relation to diallel crossing systems. Australian Journal of Biological Sciences, 9, 463–493. 
Harrell F E, Dupont C. 2016. Hmisc: Harrell miscellaneous. R package version 4.0-0. https://cran.r-project.org/web/packages/Hmisc/index.html. 
Hu H, Xiong L. 2014. Genetic engineering and breeding of drought-resistant crops. Annual Review of Plant Biology, 65, 715–741. 
Huang X, Yang S, Gong J, Zhao Y, Feng Q, Gong H, Li W, Zhan Q, Cheng B, Xia J, Chen N, Hao Z, Liu K, Zhu C, Huang T, Zhao Q, Zhang L, Fan D, Zhou C, Lu Y, et al. 2015. Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. Nature Communications, 6, 6258.
Kempthorne O, Curnow R N. 1961. The partial diallel cross. Biometrics, 17, 229–250.
Kirkham M B, Suksayretrup K, Wassom C E, Kanemasu E T. 1984. Canopy temperature of drought-resistant and drought-sensitive genotypes of maize. Maydica, 29, 287–303.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. 
Kuznetsova A, Brockhoff P B, Christensen R H B. 2017. lmerTest package: tests in linear mixed effects models. Journal of Statistical Software, 82, 1–26.
Laude T P, Carena M J. 2015. Genetic diversity and heterotic grouping of tropical and temperate maize populations adapted to the northern US Corn Belt. Euphytica, 204, 661–677. 
Lu Y, Yan J, Guimaraes C T, Taba S, Hao Z, Gao S, Chen C S, Li J, Zhang S, Vivek B S, Magorokosho C, Mugo S, Makumbi D, Parentoni S N, Shah T, Rong T, Crouch J H, Xu Y. 2009. Molecular characterization of global maize breeding germplasm based on genome-wide single nucleotide polymorphisms. Theoretical and Applied Genetics, 120, 93–115. 
Makumbi D, Assanga S, Magorokosho C, Asea G, Worku M, Bänziger M. 2018. Genetic analysis of tropical midaltitude-adapted maize populations under stress and nonstress conditions. Crop Science, 58, 1492–1507. 
Makumbi D, Betrán J F, Bänziger M, Ribaut J M. 2011. Combining ability, heterosis and genetic diversity in tropical maize (Zea mays L.) under stress and non-stress conditions. Euphytica, 180, 143–162. 
Meng Y, Yan J, Teng W, Li J. 2010. Trends in genetic diversity among widely used inbreds from 1991 to 2001 in China and application of three major germplasm groups in maize breeding. Scientia Agricultura Sinica, 43, 670–679. (in Chinese)
Menkir A, Akintunde A O. 2001. Evaluation of the performance of maize hybrids-improved open-pollinated and farmers’ local varieties under well-watered and drought stress conditions. Maydica, 46, 227–238.
Mikel M A. 2008. Genetic diversity and improvement of contemporary proprietary North American dent corn. Crop Science, 48, 1686–1695. 
Mikel M A. 2011. Genetic composition of contemporary US commercial dent corn germplasm. Crop Science, 51, 592–599. 
Nei M. 1972. Genetic distance between populations. The American Naturalist, 106, 283–292.
NeSmith D, Ritchie J. 1992. Effects of soil water-deficit during tassel emergence on development and yield components of maize (Zea mays L.). Field Crops Research, 28, 251–256.
Njeri S G, Makumbi D, Warburton M L, Diallo A, Jumbo M B,  Chemining’wa G. 2017. Genetic analysis of tropical quality protein maize (Zea mays L.) germplasm. Euphytica, 213, 261. 
Oyekunle M, Badu-Apraku B, Hearne S, Franco J. 2015. Genetic diversity of tropical early-maturing maize inbreds and their performance in hybrid combinations under drought and optimum growing conditions. Field Crops Research, 170, 55–65. 
R Core Team. 2013. R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. 
Reif J C, Hallauer A R, Melchinger A E. 2005. Heterosis and heterotic patterns in maize. Maydica, 50, 215–223.
Smith J S C, Duvick D N, Smith O S, Cooper M, Feng L. 2004. Changes in pedigree backgrounds of pioneer brand maize hybrids widely grown from 1930 to 1999. Crop Science, 44, 1935–1946.
SAS (Statistical Analysis System). 2008. Institute SAS/STAT version 9.2 user’s guide. SAS Institute, Cary, NC, USA.
Su J, Zhang F, Yang X, Feng Y, Yang X, Wu Y, Guan Z, Fang W, Chen F. 2017. Combining ability, heterosis, genetic distance and their intercorrelations for waterlogging tolerance traits in chrysanthemum. Euphytica, 213, 42. 
Suwarno W B, Pixley K V, Palacios-Rojas N, Kaeppler S M, Babu R. 2014. Formation of heterotic groups and understanding genetic effects in a provitamin A biofortified maize breeding program. Crop Science, 54, 14–24. 
Teng W, Cao J, Chen Y, Chen X, Liu X, Jing X, Zhang F, Li J. 2004. Analysis of maize heterotic groups and patterns during past decade in China. Scientia Agricultura Sinica, 37, 1804–1811. (in Chinese)
Toker C, Canci H, Yildirim T. 2007. Evaluation of perennial wild Cicer species for drought resistance. Genetic Resources and Crop Evolution, 54, 1781–1786. 
Troyer A F, Palmer L S. 2006. Background and importance of Troyer Reid corn. Crop Science, 46, 2460–2467. 
Wang H, Xu C, Liu X, Guo Z, Xu X, Wang S, Xie C, Li W, Zou C, Xu Y. 2017. Development of a multiple-hybrid population for genome-wide association studies: theoretical consideration and genetic mapping of flowering traits in maize. Scientific Reports, 6, 40239. 
Wang K, Qiu F, Larazo W, Paz M A D, Xie F. 2015. Heterotic groups of tropical indica rice germplasm. Theoretical and Applied Genetics, 128, 421–430. 
Wang Y, Wang Z, Wang Y, Wang Y, Zhang X, Lu L. 1997. Studies on the heterosis utilizing models of main maize germplasms in China. Scientia Agricultura Sinica, 30, 16–24. (in Chinese)
Wei X, Zhang J. 2018. The optimal mating distance resulting from heterosis and genetic incompatibility. Science Advances, 4, eaau5518.
Xie C, Zhang S, Li M, Li X, Hao Z, Bai L, Zhang D, Liang Y. 2007. Inferring genome ancestry and estimating molecular relatedness among 187 Chinese maize inbred lines. Journal of Genetics and Genomics, 34, 738–748.
Xu C, Ren Y, Jian Y, Guo Z, Zhang Y, Xie C, Fu J, Wang H, Wang G, Xu Y, Li P, Zou C. 2017. Development of a maize 55 K SNP array with improved genome coverage for molecular breeding. Molecular Breeding, 37, 20.
Yang Y, Sang Z, Du Q, Guo Z, Li Z, Kong X, Xu Y, Zou C. 2021. Flowering time regulation model revisited by pooled sequencing of mass selection populations. Plant Science, 304, 110797.
Yu K, Wang H, Liu X, Xu C, Li Z, Xu X, Liu J, Wang Z, Xu Y. 2020. Large-scale analysis of combining ability and heterosis for development of hybrid maize breeding strategies using diverse germplasm resources. Frontiers in Plant Science, 11, 660.
Zhang R, Xia J, Xue J, Shi G. 2004. Improvement and utilization of maize 78599 germplasm. Chinese Agricultural Science Bulletin, 20, 128–130. (in Chinese)
Zhang R, Xu G, Li J, Yan J, Li H, Yang X. 2018. Patterns of genomic variation in Chinese maize inbred lines and implications for genetic improvement. Theoretical and Applied Genetics, 131, 1207–1221. 
Zhang X, Yong H, Zhou Z, Zhang C, Lu M, Sun Q, Zhang L, Li M, Zhang D, Weng J, Hao Z, Zhang S, Wang Z, Li X. 2017. Heterosis and combining ability of seven maize germplasm populations. Euphytica, 213, 45. 
Zhang X, Zhang H, Li L, Lan H, Ren Z, Liu D, Wu L, Liu H, Jaqueth J, Li B, Pan G, Gao S. 2016. Characterizing the population structure and genetic diversity of maize breeding germplasm in Southwest China using genome-wide SNP markers. BMC Genomics, 17, 697.
Zhao Y, Li Z, Liu G, Jiang Y, Maurer H P T, Würschum T, Mock H, Matros A, Ebmeyer E, Schachschneider R, Kazman E, Schacht J, Gowda M, Login C F H, Reif J C. 2015. Genome-based establishment of a high-yielding heterotic pattern for hybrid wheat breeding. Proceedings of the National Academy of Sciences of the United States of America, 112, 15624–15629.

[1] WANG Xing-long, ZHU Yu-peng, YAN Ye, HOU Jia-min, WANG Hai-jiang, LUO Ning, WEI Dan, MENG Qing-feng, WANG Pu. Irrigation mitigates the heat impacts on photosynthesis during grain filling in maize [J]. >Journal of Integrative Agriculture, 2023, 22(8): 2370-2383.
[2] Tiago SILVA, Ying NIU, Tyler TOWLES, Sebe BROWN, Graham P. HEAD, Wade WALKER, Fangneng HUANG. Selection, effective dominance, and completeness of Cry1A.105/Cry2Ab2 dual-protein resistance in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2151-2161.
[3] FAN Ting-lu, LI Shang-zhong, ZHAO Gang, WANG Shu-ying, ZHANG Jian-jun, WANG Lei, DANG Yi, CHENG Wan-li. Response of dryland crops to climate change and drought-resistant and water-suitable planting technology: A case of spring maize[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2067-2079.
[4] ZHANG Miao-miao, DANG Peng-fei, LI Yü-ze, QIN Xiao-liang, Kadambot-H. M. SIDDIQUE. Better tillage selection before ridge–furrow film mulching can facilitate root proliferation, increase nitrogen accumulation, translocation, grain yield of maize in a semiarid area[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1658-1670.
[5] ZHANG Chong, WANG Dan-dan, ZHAO Yong-jian, XIAO Yu-lin, CHEN Huan-xuan, LIU He-pu, FENG Li-yuan, YU Chang-hao, JU Xiao-tang. Significant reduction of ammonia emissions while increasing crop yields using the 4R nutrient stewardship in an intensive cropping system[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1883-1895.
[6] WANG Peng, WANG Cheng-dong, WANG Xiao-lin, WU Yuan-hua, ZHANG Yan, SUN Yan-guo, SHI Yi, MI Guo-hua. Increasing nitrogen absorption and assimilation ability under mixed NO3 and NH4+ supply is a driver to promote growth of maize seedlings[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1896-1908.
[7] SONG Chao-yu, ZHANG Fan, LI Jian-sheng, XIE Jin-yi, YANG Chen, ZHOU Hang, ZHANG Jun-xiong. Detection of maize tassels for UAV remote sensing image with an improved YOLOX Model[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1671-1683.
[8] WANG Jin-bin, XIE Jun-hong, LI Ling-ling, ADINGO Samuel. Review on the fully mulched ridge–furrow system for sustainable maize production on the semi-arid Loess Plateau[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1277-1290.
[9] ZHAO Hai-liang, QIN Yao, XIAO Zi-yi, SUN Qin, GONG Dian-ming, QIU Fa-zhan. Revealing the process of storage protein rebalancing in high quality protein maize by proteomic and transcriptomic[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1308-1323.
[10] ZHANG Bing-chao, HU Han, GUO Zheng-yu, GONG Shuai, SHEN Si, LIAO Shu-hua, WANG Xin, ZHOU Shun-li, ZHANG Zhong-dong. Plastic-film-side seeding, as an alternative to traditional film mulching, improves yield stability and income in maize production in semi-arid regions[J]. >Journal of Integrative Agriculture, 2023, 22(4): 1021-1034.
[11] SHI Wen-xuan, ZHANG Qian, LI Lan-tao, TAN Jin-fang, XIE Ruo-han, WANG Yi-lun. Hole fertilization in the root zone facilitates maize yield and nitrogen utilization by mitigating potential N loss and improving mineral N accumulation[J]. >Journal of Integrative Agriculture, 2023, 22(4): 1184-1198.
[12] GAO Xing, LI Yong-xiang, YANG Ming-tao, LI Chun-hui, SONG Yan-chun, WANG Tian-yu, LI Yu, SHI Yun-su. Changes in grain-filling characteristics of single-cross maize hybrids released in China from 1964 to 2014[J]. >Journal of Integrative Agriculture, 2023, 22(3): 691-700.
[13] Irshad AHMAD, Maksat BATYRBEK, Khushnuma IKRAM, Shakeel AHMAD, Muhammad KAMRAN, Misbah, Raham Sher KHAN, HOU Fu-jiang, HAN Qing-fang.

Nitrogen management improves lodging resistance and production in maize (Zea mays L.) at a high plant density [J]. >Journal of Integrative Agriculture, 2023, 22(2): 417-433.

[14] XU Xiao-hui, LI Wen-lan, YANG Shu-ke, ZHU Xiang-zhen, SUN Hong-wei, LI Fan, LU Xing-bo, CUI Jin-jie. Identification, evolution, expression and protein interaction analysis of genes encoding B-box zinc-finger proteins in maize[J]. >Journal of Integrative Agriculture, 2023, 22(2): 371-388.
[15] CHEN Zhe, REN Wei, YI Xia, LI Qiang, CAI Hong-guang, Farhan ALI, YUAN Li-xing, MI Guo-hua, PAN Qing-chun, CHEN Fan-jun. Local nitrogen application increases maize post-silking nitrogen uptake of responsive genotypes via enhanced deep root growth[J]. >Journal of Integrative Agriculture, 2023, 22(1): 235-250.
No Suggested Reading articles found!