Abstract
Diverse haploid inducer lines with > 6% of haploid induction rate are now routinely used to develop doubled haploid lines. Though MTL gene regulates haploid induction, its molecular characterization and haplotype analysis in maize and its related species have not been undertaken so far. In the present study, the entire 1812 bp long MTL gene was sequenced among two mutant and eight wild-type inbreds. A 4 bp insertion differentiated the mutant from the wild-type allele. Sequence analysis further revealed 103 polymorphic sites including 38 InDels and 65 SNPs. A total of 15 conserved regions were detected, of which exon-4 was the most conserved. Ten gene-based markers specific to MTL revealed the presence of 40 haplotypes among diverse 48 inbreds of exotic and indigenous origin. It generated 20 alleles with an average of two alleles per locus. The mean polymorphic information content was 0.3247 with mean gene diversity of 0.4135. A total of 15 paralogous sequences of MTL were detected in maize genome with 3–7 exons. Maize MTL proteins of both wild-type and mutant were non-polar in nature, and they possessed four domains. R1-nj-based haploid inducer (HI) lines viz., Pusa-HI-101 and Pusa-HI-102 had an average haploid induction rate of 8.45 ± 0.96% and 10.46 ± 1.15%, respectively. Lines wild-type MTL gene did not generate any haploid. In comparison with 27 orthologues of 21 grass species, maize MTL gene had the closest ancestry with Saccharum spontaneum and Sorghum. The information generated here assumes great significance in understanding the diversity of MTL gene and presence of paralogues and orthologues. This is the first report on haplotype analysis and molecular characterization of MTL gene in maize and related grass species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All the data is available in the manuscript and supplementaryinformation.
References
Bahtiar AM, Salman D, Azrai M, Tenrirawe A, Yasin M, Gaffar A, Sebayang A, Ochieng PJ (2023) Promoting the new superior variety of national hybrid maize: improve farmer satisfaction to enhance production. Agriculture 13:174. https://doi.org/10.3390/agriculture13010174
Barret P, Brinkmann M, Beckert M (2008) A major locus expressed in the male gametophyte with incomplete penetrance is responsible for in situ gynogenesis in maize. Theor Appl Genet 117: 581–594. https://doi.org/10.1007/s00122-008-0803-6
Burke JE, Dennis EA (2009) Phospholipase A2 structure/function, mechanism, and signaling1. J Lipid Res 50: S23–S242. https://doi.org/10.1194/jlr.R800033-JLR200
Chaikam V, Nair SK, Martinez L, Lopez LA, Utz HF, Melchinger AE, Boddupalli PM (2018) Marker-assisted breeding of improved maternal haploid inducers in maize for the tropical/subtropical regions. Front Plant Sci 9:385997. https://doi.org/10.3389/fpls.2018.01527
Chaikam V, Molenaar W, Melchinger AE, Boddupalli PM (2019) Doubled haploid technology for line development in maize: technical advances and prospects. Theor Appl Genet 132: 3227–3243. https://doi.org/10.1007/s00122-019-03433-x
Chen YR, Lübberstedt T, Frei UK (2024) Development of doubled haploid inducer lines facilitates selection of superior haploid inducers in maize. Front Plant Sci 14:1320660. https://doi.org/10.3389/fpls.2023.1320660
Cheng Z, Sun Y, Yang S, Zhi H, Yin T, Ma X, Zhang H, Diao X, Guo Y, Li X, Wu C (2021) Establishing in planta haploid inducer line by edited SiMTL in foxtail millet (Setaria italica). Plant Biotechnol J 19: 1089–1091. https://doi.org/10.1111/pbi.13584
Coe EH Jr (1959) A line of maize with high haploid frequency. Am Nat 93:381–382
Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V (2004) Darwin's abominable mystery: insights from a supertree of the angiosperms. Proc Natl Acad Sci 101: 1904–1909. https://doi.org/10.1073/pnas.0308127100
Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1: 19–21. https://doi.org/10.1007/BF02712670
Dong X, Xu X, Miao J, Li L, Zhang D, Mi X, Liu C, Tian X, Melchinger AE, Chen S (2013) Fine mapping of qhir1 influencing in vivo haploid induction in maize. Theor Appl Genet 126: 1713–1720. https://doi.org/10.1007/s00122-013-2086-9
Dutta S, Muthusamy V, Zunjare RU, Bhowmick R, Hossain F (2019) Genome wide study of fatty acid hydroxylase (FAH) superfamily containing β-carotene hydroxylase (crtRB1) in maize (Zea mays L.). Pharma Innov 8:422–428
Dutta S, Muthusamy V, Zunjare RU, Hossain F (2022) Accelerated generation of elite inbreds in maize using doubled haploid technology. Plant Breeding-New Perspectives. https://doi.org/10.5772/intechopen.105824
Dutta S, Zunjare RU, Sil A, Mishra DC, Arora A, Gain N, Chand G, Chhabra R, Muthusamy V, Hossain F (2024) Prediction of matrilineal specific patatin-like protein governing in-vivo maternal haploid induction in maize using support vector machine and di-peptide composition. Amino Acids 56(1):20. https://doi.org/10.1007/s00726-023-03368-0
Dolezel J, Bartos JAN (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot 95(1):99–110. https://doi.org/10.1093/aob/mci005
Erenstein O, Jaleta M, Sonder K, Mottaleb K, Prasanna BM (2022) Global maize production, consumption and trade: trends and R&D implications. Food Secur 14: 1295–1319. https://doi.org/10.1007/s12571-022-01288-7
Gain N, Chhabra R, Chandra S, Zunjare RU, Dutta S, Chand G, Sarika K, Devi EL, Kumar A, Madhavan J, Muthusamy V, Hossain F (2022) Variation in anthocyanin pigmentation by R1-navajo gene, development and validation of breeder-friendly markers specific to C1-Inhibitor locus for in-vivo haploid production in maize. Mol Biol Rep 50: 2221–2229. https://doi.org/10.1007/s11033-022-08214-2
Gilles LM, Calhau AR, La Padula V, Jacquier NM, Lionnet C, Martinant JP, Rogowsky PM, Widiez T (2021) Lipid anchoring and electrostatic interactions target NOT-LIKE-DAD to pollen endo-plasma membrane. J Cell Biol 220: e202010077. https://doi.org/10.1083/jcb.202010077
Gilles LM, Khaled A, Laffaire JB, Chaignon S, Gendrot G, Laplaige J, Berges H, Beydon G, Bayle V, Barret P, Comadran J (2017) Loss of pollen‐specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. The EMBO journal 36: 707–717. https://doi.org/10.15252/embj.201796603
Guermeur Y, Geourjon C, Gallinari P, Deléage G (1999) Improved performance in protein secondary structure prediction by inhomogeneous score combination. Bioinformatics 15: 413–421. https://doi.org/10.1093/bioinformatics/15.5.413
Hu H, Schrag TA, Peis R, Unterseer S, Schipprack W, Chen S, Lai J, Yan J, Prasanna BM, Nair SK, Chaikam V (2016) The genetic basis of haploid induction in maize identified with a novel genome-wide association method. Genetics 202: 1267–1276. https://doi.org/10.1534/genetics.115.184234
Ishii T, Karimi-Ashtiyani R, Houben A (2016) Haploidization via chromosome elimination: means and mechanisms. Annu Rev Plant Biol 67: 421–438. https://doi.org/10.1146/annurev-arplant-043014-114714
Jacquier NM, Gilles LM, Pyott DE, Martinant JP, Rogowsky PM, Widiez T (2020) Puzzling out plant reproduction by haploid induction for innovations in plant breeding. Nat Plants 6: 610–619. https://doi.org/10.1038/s41477-020-0664-9
Jiang C, Sun J, Li R, Yan S, Chen W, Guo L, Qin G, Wang P, Luo C, Huang W, Zhang Q (2022) A reactive oxygen species burst causes haploid induction in maize. Mol Plant 15: 943–955. https://doi.org/10.1016/j.molp.2022.04.001
Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20: 1313–1326. https://doi.org/10.1101/gr.101386.109
Kelliher T, Starr D, Richbourg L, Chintamanani S, Delzer B, Nuccio ML, Green J, Chen Z, McCuiston J, Wang W, Liebler T (2017) MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542: 105–109. https://doi.org/10.1038/nature20827
Khammona K, Dermail A, Suriharn K, Lübberstedt T, Wanchana S, Thunnom B, Poncheewin W, Toojinda T, Ruanjaichon V, Arikit S (2024) Accelerating haploid induction rate and haploid validation through marker-assisted selection for qhir1 and qhir8 in maize. Front Plant Sci 15:1337463. https://doi.org/10.3389/fpls.2024.1337463
King RD, Sternberg MJ (1996) Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci 5: 2298–2310. https://doi.org/10.1002/pro.5560051116
Kozlowski LP (2016) IPC-isoelectric point calculator. Biol Direct 11: 1–16. https://doi.org/10.1186/s13062-016-0159-9
Kuhlman B, Bradley P (2019) Advances in protein structure prediction and design. Nat Rev Mol Cell Biol 20: 681–697. https://doi.org/10.1038/s41580-019-0163-x
La Camera S, Geoffroy P, Samaha H, Ndiaye A, Rahim G, Legrand M, Heitz T (2005) A pathogen‐inducible patatin‐like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 44: 810–825. https://doi.org/10.1111/j.1365-313X.2005.02578.x
Lashermes P, Beckert M (1988) Genetic control of maternal haploidy in maize (Zea mays L.) and selection of haploid inducing lines. Theor Appl Genet 76:405–410. https://doi.org/10.1007/BF00265341
Leitwein M, Duranton M, Rougemont Q, Gagnaire PA, Bernatchez L (2020) Using haplotype information for conservation genomics. Trends Ecol Evol 35: 245–258. https://doi.org/10.1016/j.tree.2019.10.012
Li L, Ji G, Ye C, Shu C, Zhang J, Liang C (2015) PlantOrDB: A genome-wide ortholog database for land plants and green algae. BMC Plant Biol 15: 1–11. https://doi.org/10.1186/s12870-015-0531-4
Li X, Meng D, Chen S, Luo H, Zhang Q, Jin W, Yan J (2017) Single nucleus sequencing reveals spermatid chromosome fragmentation as a possible cause of maize haploid induction. Nat Commun 8: 991. https://doi.org/10.1038/s41467-017-00969-8
Liu C, Li J, Chen M, Li W, Zhong Y, Dong X, Xu X, Chen C, Tian X, Chen S (2022) Development of high-oil maize haploid inducer with a novel phenotyping strategy. The Crop Journal 10(2):524–531. https://doi.org/10.1016/j.cj.2021.07.009
Liu C, Li X, Meng D, Zhong Y, Chen C, Dong X, Xu X, Chen B, Li W, Li L, Tian X (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase A generates haploid induction in maize. Mol Plant 10: 520–522. https://doi.org/10.1016/j.molp.2017.01.011
Liu C, Li W, Zhong Y, Dong X, Hu H, Tian X, Wang L, Chen B, Chen C, Melchinger AE, Chen S (2015) Fine mapping of qhir8 affecting in vivo haploid induction in maize. Theor Appl Genet 128:2507–2515. https://doi.org/10.1007/s00122-015-2605-y
Liu C, Zhong Y, Qi X, Chen M, Liu Z, Chen C, Tian X, Li J, Jiao Y, Wang D, Wang Y (2020) Extension of the in vivo haploid induction system from diploid maize to hexaploid wheat. Plant Biotechnol J 18: 316–3018. https://doi.org/10.1111/pbi.13218
Liu, K. and Muse, S.V. (2005) PowerMarker Integrated Analysis Environment for Genetic Marker Data. Bioinformatics, 21, 2128–2129. https://doi.org/10.1093/bioinformatics/bti282
Nair SK, Molenaar W, Melchinger AE, Boddupalli PM, Martinez L, Lopez LA, Chaikam V (2017) Dissection of a major QTL qhir1 conferring maternal haploid induction ability in maize. Theor Appl Genet 130: 1113–1122. https://doi.org/10.1007/s00122-017-2873-9
Nekrutenko A, Makova KD, Li WH (2002) The KA/KS ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. Genome Res 12: 198–202. https://doi.org/10.1101/gr.200901
Otto SP, Lenormand T (2002) Resolving the paradox of sex and recombination. Nat Rev Genet 3:252–261. https://doi.org/10.1038/nrg761
Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/darwin
Prasanna BM, Chaikam V, Mahuku G (2012) Doubled haploid technology in maize breeding: theory and practice. CIMMYT. http://hdl.handle.net/10883/1351
Prigge V, Schipprack W, Mahuku G, Atlin GN, Melchinger AE (2012) Development of in vivo haploid inducers for tropical maize breeding programs. Euphytica 185:481–490. https://doi.org/10.1007/s10681-012-0657-5
Randolph LF (1932) Some effects of high temperature on polyploidy and other variations in maize. Proc Natl Acad Sci U S A 18: 222–229. https://doi.org/10.1073/pnas.18.3.222
Rangari SK, Kaur Sudha M, Kaur H, Uppal N, Singh G, Vikal Y, Sharma P (2023) DNA-free genome editing for ZmPLA1 gene via targeting immature embryos in tropical maize. GM Crops and Food 14(1):1–7. https://doi.org/10.1080/21645698.2023.2197303
Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, Barford D (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature, 423: 769–773. https://doi.org/10.1038/nature01680
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol
30: 2725–2729. https://doi.org/10.1093/molbev/mst197
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Res 40: e115. https://doi.org/10.1093/nar/gks596
Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93: 77–78. https://doi.org/10.1093/jhered/93.1.77
Walbot V, Evans MM (2003) Unique features of the plant life cycle and their consequences. Nat Rev Genet 4: 369–379. https://doi.org/10.1038/nrg1064
Wang J, Cao Y, Wang K, Liu C (2022) Development of Multiple-Heading-Date mtl Haploid Inducer Lines in Rice. Agriculture 12: 806. https://doi.org/10.3390/agriculture12060806
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46: W296-W303. https://doi.org/10.1093/nar/gky427
Zhang Z, Yu J (2006) Evaluation of six methods for estimating synonymous and nonsynonymous substitution rates. Genomics Proteomics Bioinformatics 4: 173–181. https://doi.org/10.1016/S1672-0229(06)60030-2
Zhong Y, Liu C, Qi X, Jiao Y, Wang D, Wang Y, Liu Z, Chen C, Chen B, Tian X, Li J (2019) Mutation of ZmDMP enhances haploid induction in maize. Nature Plants 5(6):575–580. https://doi.org/10.1038/s41477-019-0443-7
Acknowledgements
The First author is thankful to the Human Resource Development Group (HRDG) division of the Council of Scientific & Industrial Research (CSIR), New Delhi, India for the Junior Research Fellowship (File No.: 09/083(0383)/2019-EMR-I) to pursue his Ph.D. program.
Funding
This study was funded by ICAR-IARI, New Delhi, CRP on Hybrid Technology (Maize Component) (24-142G), and Department of Biotechnology-TWIN sponsored project on ‘Development of locally adapted haploid inducer lines in maize through marker-assisted introgression of pollen-specific MATRILINEAL phospholipase gene’ [BT/PR25134/NER/95/1035/2017].
Author information
Authors and Affiliations
Contributions
Conduct of the experiment: SD; Gene diversity analysis: RC; Primer designing and protocol standardization for sequencing: VM and NG, Flow cytometry: RS, Paralogue analysis: RUZ, Orthologue analysis: JM and NG, Manuscript writing: SD and FH; Editing of manuscript: ELD, Designing of experiment: FH and KS.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dutta, S., Chhabra, R., Muthusamy, V. et al. Allelic variation and haplotype diversity of Matrilineal (MTL) gene governing in vivo maternal haploid induction in maize. Physiol Mol Biol Plants (2024). https://doi.org/10.1007/s12298-024-01456-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12298-024-01456-3