Abstract
Key message
Wheat anther-specific invertase genes were haplotyped in wheat. Strong allelic selection occurred during wheat polyploidization, domestication and breeding because of their association with yield traits.
Abstract
Plant invertase hydrolyzes sucrose into glucose and fructose. Cell wall invertase (CWI), one of the three types of invertase, is essential for plant development. Based on isolated TaCWI genes from chromosomes 4A, 5B and 5D, two SNPs were detected in the promoter region of TaCWI-4A, and four SNPs and two Indels were present in the TaCWI-5D gene. No polymorphism was detected in TaCWI-5B coding or promoter regions. CAPS markers caps4A and caps5D were developed to discriminate haplotypes of TaCWI-4A and TaCWI-5D. Marker/trait association analysis indicated that Hap-5D-C at TaCWI-5D was significantly associated with higher thousand kernel weight (TKW) in 348 Chinese modern cultivars grown in multiple environments. Geographic distributions and changes over time of favored haplotypes showed that Hap-5D-C was the most frequent haplotype in modern cultivars and was strongly positively selected in six major wheat production regions worldwide. However, selection for haplotypes at TaCWI-4A was not so evident, possibly due to balancing effects of the two haplotypes on TKW and grain number per spike (GN). In rainfed production regions, Hap-4A-C was favored because it brought more seeds, but in well irrigated conditions, Hap-4A-T was favored in modern breeding because of higher TKW. Evolutionary analysis among wheat and its relatives showed that genetic diversity of TaCWI genes on chromosomes 4A and 5D declined dramatically in progression from the diploid level to modern polyploid cultivars. There was strong allelic selection during polyploidization, domestication and breeding.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
One-way analysis of variance
- ETN:
-
Effective tiller number
- GN:
-
Grain number per spike
- HD:
-
Heading date
- MD:
-
Maturity date
- PH:
-
Plant height
- TKW:
-
Thousand kernel weight
- SpL:
-
Spike length
References
Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37:859–869
Bordes J, Ravel C, Jaubertie JP, Duperrier B, Gardet O, Heumez E, Pissavy AL, Charmet G, Le Gouis J, Balfourier F (2013) Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection. Theor Appl Genet 126:805–822
Boter M, Ruíz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591
Chen DH, Ronalds PC (1999) Rapid DNA mini preparation method suitable for AFLP and other PCR applications. Plant Mol Biol Rep 17:53–57
Cheng WH, Taliercio EW, Chourey PS (1996) The miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–983
Cho J, Kyu S, Lee SK (2005) Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.). Plant Cell Rep 24:225–236
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Copenald L (1990) Enzyme of sucrose metabolism. Methods Plant Biochem 3:73–85
Dong YS, Cao YS, Zhang XY, Liu SC, Wang LF, You GX, Pang BS, Li LH, Jia JZ (2003) Development of candidate core collections in Chinese common wheat germplasm. J Plant Genet Resources 4:1–8 (in Chinese)
Dorion S, Lalonde S, Saini HS (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111:137–145
Hanocq E, Laperche A, Jaminon O, Lainé A, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584
Hao CY, Dong YC, Wang LF, You GX, Zhang HN, Ge HM, Jia JZ, Zhang XY (2008) Genetic diversity and construction of core collection in Chinese wheat genetic resources. Chinese Sci Bull 53:1518–1526
Hao CY, Wang LF, Ge HM, Dong YC, Zhang XY (2011) Genetic diversity and linkage disequilibrium in Chinese bread wheat (Triticum aestivum L.) revealed by SSR markers. PLoS One 6:e17279
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Hou J, Jiang QY, Hao CY, Wang YQ, Zhang HN, Zhang XY (2014) Global selection on sucrose synthase haplotypes during a century of wheat breeding. Plant Physiol 164:1918–1929
Ji XM, Shiran B, Wan JL, Lewis DC, Jenkins CLD, Condon AG, Richard AR, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ 33:926–942
Jia JZ, Zhao SC, Kong XY, Li YR, Zhao GY et al (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95
Kang BH, Xiong YQ, Williams DS, Pozueta-Romero D, Chourey PS (2009) Miniature1-encoded cell wall invertase is essential for assembly and function of wall-in-growth in the maize endosperm transfer cell. Plant Physiol 151:1366–1376
Kim JY, Mahéa A, Guya S, Brangeona J, Rochea O, Choureyb PS, Prioula JL (2000) Characterization of two members of the maize gene family, Incw3 and Incw4, encoding cell-wall invertases. Gene 245:89–102
King G, Nienhuis J, Hussey C (1993) Genetic similarity among ecotypes of Arabidopsis thaliana estimated by analysis of restriction fragment length polymorphisms. Theor Appl Genet 86:1028–1032
Koonjul PK, Minhas JS, Nunes C, Sheoran IS, Saini HS (2005) Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. J Exp Bot 56:179–190
Kumar S, Nei M, Joel D, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306
Kumbhar MB, Larik AS, Hafiz HMI, Rind MJ (1983) Interrelationship of polygenic traits affecting grain yield in Triticum aestivum L. Wheat Information Service 57:42–45
Liu CJ, Atkinson MD, Chinoy CN, Devos KM, Gale MD (1992) Nonhomoeologous translocations between group 4, 5 and 7 chromosomes within wheat and rye. Theor Appl Genet 83:305–312
Ma DY, Yan J, He ZH, Wu L, Xia XC (2012) Characterization of a cell wall invertase gene TaCwi-A1 on common wheat chromosome 2A and development of functional markers. Mol Breeding 29:43–52
Miller ME, Chourey PS (1992) The maize invertase-deficient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4:297–305
Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao XC, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28:1534–1551
Peng JR, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261
Qin L, Hao CY, Hou J, Wang YQ, Wang YQ, Li T, Wang LF, Ma ZQ, Zhang XY (2014) Homologous haplotypes, expression, genetic effects and geographic distribution of the wheat yield gene TaGW2. BMC Plant Biol 14:107
Rogers HJ, Bate N, Combe J, Sullivan J, Sweetman J, Swan C, Lonsdale DM, Twell D (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45:577–585
Sturm A (1996) Molecular characterization and functional analysis of sucrose-cleaving enzymes in carrot (Daucus carota L.). J Exp Bot 47:1187–1192
Sturm A (1999) Invertases, primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7
Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407
Tang GQ, Luscher M, Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11:177–189
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tian JC, Deng ZY, Hu RB, Wang YX (2006) Yield components of super wheat cultivars with different types and the path coefficient analysis on grain yield. Acta Agron Sin 32:1699–1705
Tymowska-Lalanne Z, Kreis M (1998) The plant invertases: physiology, biochemistry and molecular biology. Adv Bot Res 28:70–117
Vincze T, Posfai J, Roberts RJ (2003) NEBcutter: a program to cleave DNA with restriction enzymes. Nucleic Acids Res 31:3688–3691
Wang ET, Wang JJ, Zhu XD, Hao W, Wang LY, Li Q, Zhang LX, He W, Lu BR, Lin HX, Ma H, Zhang GQ, He ZH (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374
Webster H, Keeble G, Dell B, Fosu-Nyarko J, Mukai Y, Moolhuijzen P, Bellgard M, Jia JZ, Kong XY, Feuillet C, Frédéric C, Appels R (2012) Genome-level identification of cell wall invertase genes in wheat for the study of drought tolerance. Funct Integr Genomics 39:569–579
Zhang XY, Li CW, Wang LF, Wang HM, You GX, Dong YS (2002) An estimation of the minimum number of SSR alleles needed to reveal genetic relationships in wheat varieties information from large-scale planted varieties and cornerstone breeding parents in Chinese wheat improvement and production. Theor Appl Genet 106:112–117
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 1960–2000. Crop Sci 47:245–253
Zhuang QS (2003) Chinese wheat improvement and pedigree analysis. Agricultural Press Beijing (in Chinese)
Acknowledgments
We thank Dr. D.C. Liu, Institute of Genetics and Developmental Biology, Chinese Academy of Science and Dr. SL Xue, Nanjing Agricultural University, for their help in mapping of the TaCWI-4A and TaCWI-5D, respectively. We also gratefully acknowledge help from Prof. Robert A McIntosh, University of Sydney in English editing. This research was supported by Chinese Ministry of Science and Technology (grant no. 2010CB125900), the Animal and Plant Transgenic Project (2013ZX08009-001) and CAAS Innovation Project.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by Mark E. Sorrells.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jiang, Y., Jiang, Q., Hao, C. et al. A yield-associated gene TaCWI, in wheat: its function, selection and evolution in global breeding revealed by haplotype analysis. Theor Appl Genet 128, 131–143 (2015). https://doi.org/10.1007/s00122-014-2417-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-014-2417-5