Abstract
Main conclusion
This study explored 6P chromosomal translocations in wheat, and determined the effects of 6P intercalary chromosome segments on kernel number per wheat spike.
Exploiting and utilising gene(s) from wild relative species has become an essential strategy for wheat crop improvement. In the translocation line Pubing2978, the intercalary 6P chromosome segment from Agropyron cristatum (L.) Gaertn. (2n = 4x = 28, PPPP) carried valuable multi-kernel gene(s) and was selected from the offspring of the common wheat plant Fukuho and the irradiated wheat-A. cristatum 6P disomic substitution line 4844-8. Genomic in situ hybridisation (GISH), dual-colour fluorescence in situ hybridisation (FISH), and molecular markers were used to detect the small segmental 6P chromosome in the wheat background and its translocation breakpoint. Cytological studies demonstrated that Pubing2978 was a T1AS-6PL-1AS·1AL intercalary translocation with 42 chromosomes. The breakpoint was located near the centromeric region on the wheat chromosome 1AS and was flanked by the markers SSR12 and SSR283 based on an F2 linkage map. The genotypic data, combined with the phenotypic information, implied that A. cristatum 6P chromosomal segment plays an important role in regulating the kernel number per spike (KPS). By comparison, the mean value of KPS in plants with translocations was approximately 10 higher than that in plants without translocations in three segregated populations. Moreover, the improvement in KPS was likely achieved by increasing both the spikelet number per spike (SNS) and the kernel number per spikelet. These excellent agronomic traits laid the foundation for further investigation of valuable genes and make the Pubing2978 line a promising germplasm for wheat breeding.





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- FISH:
-
Fluorescence in situ hybridisation
- GISH:
-
Genomic in situ hybridisation
- Fukuho:
-
Wheat cv. Fukuhokomugi
- KPS:
-
Kernel number per spike
- SNS:
-
Spikelet number per spike
- KNS:
-
Kernel number per spikelet
- SL:
-
Spike length
References
Allen GC, Flores-Vergara MA, Krasynanski S, Kumar S, Thompson WF (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 1:2320–2325. doi:10.1038/nprot.2006.384
Araki E, Miura H, Sawada S (1999) Identification of genetic loci affecting amylose content and agronomic traits on chromosome 4A of wheat. Theor Appl Genet 98:977–984. doi:10.1007/s001220051158
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745. doi:10.1126/science.1113373
Boden SA, Cavanagh C, Cullis BR, Ramm K, Greenwood J, Jean Finnegan E, Trevaskis B, Swain SM (2015) Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nature Plants 1:14016. doi:10.1038/nplants.2014.16
Bommert P, Nardmann J, Vollbrecht E, Running M, Jackson D, Hake S, Werr W (2005) Thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132:1235–1245
Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder M, Weber W (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936. doi:10.1007/s00122-002-0994-1
Bryan GJ, Collins AJ, Stephenson P, Orry A, Smith JB, Gale MD (1997) Isolation and characterisation of microsatellites from hexaploid bread wheat. Theor Appl Genet 94:557–563. doi:10.1007/s001220050451
Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci USA 108:7727–7732. doi:10.1073/pnas.1016981108
Chapman C (1989) Collection strategies for the wild relatives of field crops. The use of plant genetic resources. Cambridge University Press, Cambridge, pp 263–279
Chen P, You C, Hu Y, Chen S, Zhou B, Cao A, Wang X (2013) Radiation-induced translocations with reduced Haynaldia villosa chromatin at the Pm21 locus for powdery mildew resistance in wheat. Mol Breeding 31:477–484. doi:10.1007/s11032-012-9804-x
Cuadrado A, Schwarzacher T, Jouve N (2000) Identification of different chromatin classes in wheat using in situ hybridization with simple sequence repeat oligonucleotides. Theor Appl Genet 101:711–717. doi:10.1007/s001220051535
Cuthbert JL, Somers DJ, Brûlé-Babel AL, Brown PD, Crow GH (2008) Molecular mapping of quantitative trait loci for yield and yield components in spring wheat (Triticum aestivum L.). Theor Appl Genet 117:595–608. doi:10.1007/s00122-008-0804-5
Deng S, Wu X, Wu Y, Zhou R, Wang H, Jia J, Liu S (2011) Characterization and precise mapping of a QTL increasing spike number with pleiotropic effects in wheat. Theor Appl Genet 122:281–289. doi:10.1007/s00122-010-1443-1
Dewey DR (1984) The genomic system of classification as a guide to intergeneric hybridization with the perennial Triticeae. In: Gustafson JP (ed) Gene manipulation in plant improvement Proceedings of 16th Stadler Genetics Symposium, New York, pp 209–279. doi:10.1007/978-1-4613-2429-4_9
Dobrovolskaya O, Pont C, Sibout R, Martinek P, Badaeva E, Murat F, Chosson A, Watanabe N, Prat E, Gautier N, Gautier V, Poncet C, Orlov YL, Krasnikov AA, Bergès H, Salina E, Laikova L, Salse J (2015) FRIZZY PANICLE drives supernumerary spikelets in bread wheat. Plant Physiol 167:189–199. doi:10.1104/pp.114.250043
Dong Y, Zhou R, Xu S, Li L, Cauderon Y, Wang R (1992) Desirable characteristics in perennial Triticeae collected in China for wheat improvement. Hereditas 116:175–178
Du W, Wang J, Pang Y, Li Y, Chen X, Zhao J, Yang Q, Wu J (2013) Isolation and characterization of a Psathyrostachys huashanica Keng 6Ns chromosome addition in common wheat. PLoS ONE 8:e53921. doi:10.1371/journal.pone.0053921
Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866. doi:10.1126/science.1143986
Frederick JR, Bauer PJ (1999) Physiological and numerical components of wheat yield. In: Satorre EH, Slafer GA (eds) Wheat: ecology and physiology of yield determination. Food Products Press, New York, pp 45–65
Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91:59–87. doi:10.1007/BF00035277
Gaju O, Reynolds MP, Sparkes DL, Foulkes MJ (2009) Relationships between large-spike phenotype, grain number, and yield potential in spring wheat. Crop Sci 49:961–973. doi:10.2135/cropsci2008.05.0285
Gill BS, Appels R, Botha-Oberholster A-M, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvořák J, Iwanaga M, Keller B, Li W, McCombie WR, Ogihara Y, Quetier F, Sasaki T (2004) A workshop report on wheat genome sequencing: International Genome Research on Wheat Consortium. Genetics 168:1087–1096. doi:10.1534/genetics.104.034769
Grafius JE (1978) Multiple characters and correlated response. Crop Sci 18:931–934. doi:10.2135/cropsci1978.0011183X001800060004x
Guo B (1987) Chinese plant log. Chinese Scientific Press, Beijing
Gupta PK, Mir RR, Mohan A, Kumar J (2008) Wheat genomics: present status and future prospects. Int J Plant Genomics 2008:896451. doi:10.1155/2008/896451
Han F, Liu B, Fedak G, Liu Z (2004) Genomic constitution and variation in five partial amphiploids of wheat-Thinopyrum intermedium as revealed by GISH, multicolor GISH and seed storage protein analysis. Theor Appl Genet 109:1070–1076. doi:10.1007/s00122-004-1720-y
Han H, Bai L, Su J, Zhang J, Song L, Gao A, Yang X, Li X, Liu W, Li L (2014) Genetic rearrangements of six wheat-Agropyron cristatum 6P addition lines revealed by molecular markers. PLoS ONE 9:e91066. doi:10.1371/journal.pone.0091066
Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glémin S, David J (2007) Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol 24:1506–1517. doi:10.1093/molbev/msm077
Huang XQ, Kempf H, Ganal MW, Röder MS (2004) Advanced backcross QTL analysis in progenies derived from a cross between a German elite winter wheat variety and a synthetic wheat (Triticum aestivum L.). Theor Appl Genet 109:933–943. doi:10.1007/s00122-004-1708-7
Huang C, J-p Zhang, W-h Liu, X-m Yang, Li X-q Lu, Y-q Li L-h, A-n Gao (2013) Identification of wheat-Agropyron cristatum 6P chromosome intercalary translocation lines. J Plant Genet Resour 14:606–611
Jia J (1984) The statistical analysis for correlation factors in kernel weight and plant characters in wheat (T. aestivum L.). Acta Agron Sin 10:201–205
Kato K, Miura H, Sawada S (2000) Mapping QTLs controlling grain yield and its components on chromosome 5A of wheat. Theor Appl Genet 101:1114–1121. doi:10.1007/s001220051587
Kumar N, Kulwal PL, Balyan HS, Gupta PK (2007) QTL mapping for yield and yield contributing traits in two mapping populations of bread wheat. Mol Breeding 19:163–177. doi:10.1007/s11032-006-9056-8
Li L (1995) Cytogenetics and self-fertility of hybrids between Triticum aestivum L. and Agropyron cristatum (L.) Gaertn. Chin J Genet 22:105–112
Li Z, Rong S, Chen S, Zhong G, Mu S (1985) Wheat wide hybridization. Chinese Scientific Press, Beijing
Li L, Yang X, Li X, Dong Y, Chen X (1998a) Introduction of desirable genes from Agropyron cristatum into common wheat by intergeneric hybridization. Sci Agric Sin 31:1–6
Li L, Yang X, Zhou R, Li X, Dong Y (1998b) Establishment of wheat-Agropyron cristatum alien addition lines II. Identification of alien chromosomes and analysis of development approaches. Acta Genetica Sinica 25:538–544
Liu R, Meng J (2003) [MapDraw: a Microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data]. Yi Chuan = Hereditas/Zhongguo yi chuan xue hui bian ji 25:317–321
Liu W-H, Luan Y, Wang J-C, Wang X-G, Su J-J, Zhang J-P, Yang X-M, Gao A-N, Li L-H (2010) Production and identification of wheat-Agropyron cristatum (1.4P) alien translocation lines. Genome 53:472–481. doi:10.1139/g10-023
Luan Y, Wang X, Liu W, Li C, Zhang J, Gao A, Wang Y, Yang X, Li L (2010) Production and identification of wheat-Agropyron cristatum 6P translocation lines. Planta 232:501–510. doi:10.1007/s00425-010-1187-9
Ma Z, Zhao D, Zhang C, Zhang Z, Xue S, Lin F, Kong Z, Tian D, Luo Q (2007) Molecular genetic analysis of five spike-related traits in wheat using RIL and immortalized F2 populations. Mol Genet Genomics 277:31–42. doi:10.1007/s00438-006-0166-0
Millet E (1983) Breeding for large number of spikelets per spike in wheat. Proceedings of the Sixth International Wheat Genetics Symposium/Edited by Sadao Sakamoto. Kyoto: Plant Germ-Plasm Institute, Faculty of Agriculture, Kyoto University
Miura K, Ikeda M, Matsubara A, Song X-J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549. doi:10.1038/ng.592
Mohammed YS, Tahir IS, Kamal NM, Eltayeb AE, Ali AM, Tsujimoto H (2014) Impact of wheat-Leymus racemosus added chromosomes on wheat adaptation and tolerance to heat stress. Breed Sci 63:450–460. doi:10.1270/jsbbs.63.450
Narasimhamoorthy B, Gill BS, Fritz AK, Nelson JC, Brown-Guedira GL (2006) Advanced backcross QTL analysis of a hard winter wheat × synthetic wheat population. Theor Appl Genet 112:787–796. doi:10.1007/s00122-005-0159-0
Niu Z, Klindworth DL, Friesen TL, Chao S, Jin Y, Cai X, Xu SS (2011) Targeted introgression of a wheat stem rust resistance gene by DNA marker-assisted chromosome engineering. Genetics 187:1011–1021. doi:10.1534/genetics.110.123588
Ortiz R, Braun H, Crossa J, Crouch JH, Davenport G, Dixon J, Dreisigacker S, Duveiller E, He Z, Huerta J, Joshi AK, Kishii M, Kosina P, Manes Y, Mezzalama M, Morgounov A, Murakami J, Nicol J, Ortiz Ferrara G, Ortiz-Monasterio JI (2008) Wheat genetic resources enhancement by the International Maize and Wheat Improvement Center (CIMMYT). Genet Resour Crop Evol 55:1095–1140. doi:10.1007/s10722-008-9372-4
Pedersen C, Langridge P (1997) Identification of the entire chromosome complement of bread wheat by two-colour FISH. Genome 40:589–593. doi:10.1139/g97-077
Rayburn AL, Gill BS (1986) Isolation of a D-genome specific repeated DNA sequence from Aegilops squarrosa. Plant Mol Biol Rep 4:102–109. doi:10.1007/BF02732107
Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 110:859–864. doi:10.1007/s00122-004-1881-8
Röder MS, Huang X-Q, Börner A (2008) Fine mapping of the region on wheat chromosome 7D controlling grain weight. Funct Integr Genomics 8:79–86. doi:10.1007/s10142-007-0053-8
Sarhan F (2015) Wheat yields: doubling-up on grain numbers. Nature Plants. doi:10.1038/nplants.2015.3
Suzaki T, Sato M, Ashikari M, Miyoshi M, Nagato Y, Hirano H-Y (2004) The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131:5649–5657
Taguchi-Shiobara F, Yuan Z, Hake S, Jackson D (2001) The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev 15:2755–2766. doi:10.1101/gad.208501
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066. doi:10.1126/science.277.5329.1063
Tian F, Zhu Z, Zhang B, Tan L, Fu Y, Wang X, Sun CQ (2006) Fine mapping of a quantitative trait locus for grain number per panicle from wild rice (Oryza rufipogon Griff.). Theor Appl Genet 113:619–629. doi:10.1007/s00122-006-0326-y
Trethowan RM, Mujeeb-Kazi A (2008) Novel germplasm resources for improving environmental stress tolerance of hexaploid wheat. Crop Sci 48:1255–1265. doi:10.2135/cropsci2007.08.0477
Wang R (2004) Cytological and molecular characterization of a set of wheat-A. cristatum disomic addition lines. Doctoral Dissertation. Chinese Academy of Agricultural Sciences. In Chinese
Wang L, Chen P, Wang X (2010) Molecular cytogenetic analysis of Triticum aestivum-Leymus racemosus reciprocal chromosomal translocation T7DS·5LrL/T5LrS·7DL. Chin Sci Bull 55:1026–1031. doi:10.1007/s11434-010-0105-7
Wu J, Yang X, Wang H, Li H, Li L, Li X, Liu W (2006) The introgression of chromosome 6P specifying for increased numbers of florets and kernels from Agropyron cristatum into wheat. Theor Appl Genet 114:13–20. doi:10.1007/s00122-006-0405-0
Wu X, Cheng R, Xue S, Kong Z, Wan H, Li G, Huang Y, Jia H, Jia J, Zhang L, Ma Z (2014) Precise mapping of a quantitative trait locus interval for spike length and grain weight in bread wheat (Triticum aestivum L.). Mol Breeding 33:129–138. doi:10.1007/s11032-013-9939-4
Yang G, Yang X, Wang R, Gao A, Li L, Liu W (2010) The inhibiting effect of 1·4 recombinant P chromosome of wheat-Agropyron cristatum addition line on the Ph gene. Chin Sci Bull 55:153–157. doi:10.1007/s11434-010-0007-8
Yen C, Zheng Y, Yang J (1993) An ideotype for high yield breeding in theory and practice. Proceedings of 8th International Wheat Genetics Symposium Agricultural Scitech Press, Beijing, pp 1113–1117
Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989. doi:10.1038/35103589
Zhang D, Yuan Z (2014) Molecular control of grass inflorescence development. Ann Rev Plant Biol 65:553–578. doi:10.1146/annurev-arplant-050213-040104
Zhang J, Liu W, Han H, Song L, Bai L, Gao Z, Zhang Y, Yang X, Li X, Gao A, Li L (2015a) De novo transcriptome sequencing of Agropyron cristatum to identify available gene resources for the enhancement of wheat. Genomics 106:129–136. doi:10.1016/j.ygeno.2015.04.003
Zhang J, Zhang J, Liu W, Han H, Lu Y, Yang X, Li X, Li L (2015b) Introgression of Agropyron cristatum 6P chromosome segment into common wheat for enhanced thousand-grain weight and spike length. Theor Appl Genet 128:1827–1837. doi:10.1007/s00122-015-2550-9
Zhang R, Hou F, Feng Y, Zhang W, Zhang M, Chen P (2015c) Characterization of a Triticum aestivum-Dasypyrum villosum T2VS·2DL translocation line expressing a longer spike and more kernels traits. Theor Appl Genet 128:2415–2425. doi:10.1007/s00122-015-2596-8
Zhang Y, Zhang J, Huang L, Gao A, Zhang J, Yang X, Liu W, Li X, Li L (2015d) A high-density genetic map for P genome of Agropyron Gaertn. based on specific-locus amplified fragment sequencing (SLAF-seq). Planta 242:1335–1347. doi:10.1007/s00425-015-2372-7
Zheng TC, Zhang XK, Yin GH, Wang LN, Han YL, Chen L, Huang F, Tang JW, Xia XC, He ZH (2011) Genetic gains in grain yield, net photosynthesis and stomatal conductance achieved in Henan Province of China between 1981 and 2008. Field Crops Res 122:225–233. doi:10.1016/j.fcr.2011.03.015
Zhou Y, He ZH, Sui XX, Xia XC, Zhang XK, Zhang GS (2007) Genetic improvement of grain yield and associated traits in the northern China winter wheat region from 1960 to 2000. Crop Sci 47:245–253. doi:10.2135/cropsci2006.03.0175
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This work was supported by grants from the National Science and Technology Support Program of China (Grant No. 2013BAD01B02) and the National High Technology Research and Development Program of China (863 Grant No. 2011AA100101).
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Zhang, J., Zhang, J., Liu, W. et al. An intercalary translocation from Agropyron cristatum 6P chromosome into common wheat confers enhanced kernel number per spike. Planta 244, 853–864 (2016). https://doi.org/10.1007/s00425-016-2550-2
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DOI: https://doi.org/10.1007/s00425-016-2550-2


