Abstract
Doubled haploid (DH) breeding is a powerful technique to ensure global food security via accelerated crop improvement. DH can be produced in planta by employing haploid inducer stock (HIS). Widely used HIS in maize is known to be governed by ZmPLA, ZmDMP, ZmPLD3, and ZmPOD65 genes. To develop such HIS in rice and wheat, we have identified putative orthologs of these genes using in silico approaches. The OsPLD1; TaPLD1, and OsPOD6; TaPOD8 were identified as putative orthologs of ZmPLD3 and ZmPOD65 in rice and wheat, respectively. Despite being closely related to ZmPLD3, OsPLD1 and TaPLD1 have shown higher anther-specific expression. Similarly, OsPOD6 and TaPOD8 were found closely related to the ZmPOD65 based on both phylogenetic and expression analysis. However, unlike ZmPLD3 and ZmPOD65, two ZmDMP orthologs have been found for each crop. OsDMP1 and OsDMP2 in rice and TaDMP3 and TaDMP13 in wheat have shown similarity to ZmDMP in terms of both sequence and expression pattern. Furthermore, analogs to maize DMP proteins, these genes possess four transmembrane helices making them best suited to be regarded as ZmDMP orthologs. Modifying these predicted orthologous genes by CRISPR/Cas9-based genome editing can produce a highly efficient HIS in both rice and wheat. Besides revealing the genetic mechanism of haploid induction, the development of HIS would advance the genetic improvement of these crops.
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References
Aboobucker SI, Zhou L, Lübberstedt T (2023) Haploid male fertility is restored by parallel spindle genes in Arabidopsis thaliana. Nat Plants 9:1–5. https://doi.org/10.1038/s41477-022-01332-6
Ani KJ, Anyika VO, Mutambara E (2022) The impact of climate change on food and human security in Nigeria. Int J Clim Chang 14(2):148–167. https://doi.org/10.1108/IJCCSM-11-2020-0119
Anonymous (2008) Central Rice Research Institute (CRRI) Annual Report-2007–2008. National Rice Research Institute, India
Anonymous (2010) Central Rice Research Institute (CRRI) Annual Report-2009–2010. National Rice Research Institute, India
Baranwal V, Sharma SK, Ghosh A, Gupta N, Singh AK, Diksha D, Jangra TP, S (2022) Evidence for association of southern rice black-streaked dwarf virus with the recently emerged stunting disease of rice in North-West India. Indian J Genet Plant Breed 82(04):512–516
Basu U, Ahmed SR, Bhat BA, Anwar Z, Ali A, Ijaz A, Gulzar A, Bibi A, Tyagi A, Nebapure SM, Goud CA (2023) A CRISPR way for accelerating cereal crop improvement: Progress and challenges. Front Genet 13:866976. https://doi.org/10.3389/fgene.2022.866976
Chen Y, Marek GW, Marek TH, Moorhead JE, Heflin KR, Brauer DK, Gowda PH, Srinivasan R (2019) Simulating the impacts of climate change on hydrology and crop production in the Northern High Plains of Texas using an improved SWAT model. Agric Water Manag 221:13–24. https://doi.org/10.1016/j.agwat.2019.04.021
Coe JEH (1959) A line of maize with high haploid frequency. Am Nat 93(873):381–382. https://doi.org/10.1086/282098
Comai L, Tan EH (2019) HI and genome instability. Trends Genet 35(11):791–803. https://doi.org/10.1016/j.tig.2019.07.005
Cook RC (1936) A haploid Marglobe tomato: practical application of a “short cut” for making pure lines. J Hered 27:433–435. https://doi.org/10.1093/oxfordjournals.jhered.a104153
De Buyser J, Henry Y, Lonnet P, Hertzog R, Hespel A (1987) Florin: a doubled haploid wheat variety developed by the anther culture method. Plant Breed 98(1):53–56. https://doi.org/10.1111/j.1439-0523.1987.tb01089.x
Gilles LM, Khaled A, Laffaire JB, Chaignon S, Gendrot G, Laplaige J, Bergès H, Beydon G, Bayle V, Barret P, Comadran J (2017) Loss of pollen‐specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. EMBO J 36(6):707–717. https://doi.org/10.15252/embj.201796603
Ho KM, Jones GE (1980) Mingo barley. Can J Plant Sci 60:279–280. https://doi.org/10.4141/cjps80-041
Hougas RW, Peloquin SJ (1958) The potential of potato haploids in breeding and genetic research. Am Potato J 35(10):701–707. https://doi.org/10.1007/BF02855564
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(6):943–955. https://doi.org/10.1016/j.molp.2022.04.001
Kalinowska K, Chamas S, Unkel K, Demidov D, Lermontova I, Dresselhaus T, Kumlehn J, Dunemann F, Houben A (2019) State-of-the-art and novel developments of in vivo haploid technologies. Theor Appl Genet 132:593–605. https://doi.org/10.1007/s00122-018-3261-9
Kang X, Qi J, Li S, Meng FR (2022) A watershed-scale assessment of climate change impacts on crop yields in Atlantic Canada. Agric Water Manag 269:107680. https://doi.org/10.1016/j.agwat.2022.107680
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(7639):105–109. https://doi.org/10.1038/nature20827
Kelliher T, Starr D, Su X, Tang G, Chen Z, Carter J, Wittich PE, Dong S, Green J, Burch E, McCuiston J (2019) One-step genome editing of elite crop germplasm during haploid induction. Nat Biotechnol 37(3):287–292. https://doi.org/10.1038/s41587-019-0038-x
Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V (2019) A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565(7737):91–95. https://doi.org/10.1038/s41586-018-0785-8
Kolde R (2012) Pheatmap: pretty heatmaps. R Package Version 1.0.10. https://CRAN.R-project.org/package=pheatmap
Kunihisa M, Takita Y, Yamaguchi N, Okada H, Sato M, Komori S, Nishitani C, Terakami S, Yamamoto T (2019) The use of a fertile doubled haploid apple line for QTL analysis of fruit traits. Breed Sci 69(3):410–419. https://doi.org/10.1270/jsbbs.18197
Kuppu S, Ron M, Marimuthu MP, Li G, Huddleson A, Siddeek MH, Terry J, Buchner R, Shabek N, Comai L, Britt AB (2020) A variety of changes, including CRISPR/Cas9-mediated deletions, in CENH3 lead to haploid induction on outcrossing. Plant Biotechnol J 18(10):2068–2080. https://doi.org/10.1111/pbi.13365
Kyum M, Kaur H, Kamboj A, Goyal L, Bhatia D (2021) Strategies and prospects of haploid induction in rice (Oryza sativa). Plant Breed 141(1):1–11
Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, Moraes I, Koszegi D, Schubert I (2011) Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J 68(1):40–50. https://doi.org/10.1111/j.1365-313X.2011.04664.x
Li Y, Lin Z, Yue Y, Zhao H, Fei X, Liu C, Chen S, Lai J, Song W (2021) Loss-of-function alleles of ZmPLD3 cause haploid induction in maize. Nat Plants 7(12):1579–1588. https://doi.org/10.1038/s41477-021-01037-2
Li Y, Li D, Xiao Q, Wang H, Wen J, Tu J, Shen J, Fu T, Yi B (2022) An in planta haploid induction system in Brassica napus. J Integr Plant Biol 64(6):1140–1144. https://doi.org/10.1111/jipb.13270
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(3):520–522. https://doi.org/10.1016/j.molp.2017.01.011
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(2):316. https://doi.org/10.1111/pbi.13218
Lv J, Yu K, Wei J, Gui H, Liu C, Liang D, Wang Y, Zhou H, Carlin R, Rich R, Lu T (2020) Generation of paternal haploids in wheat by genome editing of the centromeric histone CENH3. Nat Biotechnol 38(12):1397–1401. https://doi.org/10.1038/s41587-020-0728-4
Madeira F, Pearce M, Tivey AR, Basutkar P, Lee J, Edbali O, Madhusoodanan N, Kolesnikov A, Lopez R (2022) Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res 50(W1):W276–W279
Meyers B, Zaltsman A, Lacroix B, Kozlovsky SV, Krichevsky A (2010) Nuclear and plastid genetic engineering of plants: comparison of opportunities and challenges. Biotechnol Adv 28(6):747–756. https://doi.org/10.1016/j.biotechadv.2010.05.022
Mhamdi A, Van Breusegem F (2018) Reactive oxygen species in plant development. Development 145(15): dev164376. https://doi.org/10.1242/dev.164376
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer EL, Tosatto SC, Paladin L, Raj S, Finn RLJ, RD (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49(D1):D412–D419. https://doi.org/10.1093/nar/gkaa913
Mushtaq M, Ahmad Dar A, Skalicky M, Tyagi A, Bhagat N, Basu U, Bhat BA, Zaid A, Ali S, Dar TUH, Rai GK (2021) CRISPR-based genome editing tools: Insights into technological breakthroughs and future challenges. Genes 12(6):797. https://doi.org/10.3390/genes12060797
Omasits U, Ahrens CH, Müller S, Wollscheid B (2014) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30(6):884–886. https://doi.org/10.1093/bioinformatics/btt607
Pearson WR (2013) An introduction to sequence similarity (“homology”) searching. Curr Protoc Bioinform 42(1):3–1. https://doi.org/10.1002/0471250953.bi0301s42
Pretini N, Vanzetti LS, Terrile II, Donaire G, González FG (2021) Mapping QTL for spike fertility and related traits in two doubled haploid wheat (Triticum aestivum L.) populations. BMC Plant Biol 21:1–8. https://doi.org/10.1186/s12870-021-03061-y
Ravi M, Chan SW (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464(7288):615–618. https://doi.org/10.1038/nature08842
Sears ER (1939) Cytogenetic studies with polyploid species of wheat. I. Chromosomal aberrations in the progeny of a haploid of Triticum vulgare. Genetics 24(4):509. https://doi.org/10.1093/genetics/24.4.509
Shi Z, Song W, Xing J, Duan M, Wang F, Tian H, Xu L, Wang S, Su A, Li C, Zhang R (2017) Molecular mapping of quantitative trait loci for three kernel-related traits in maize using a double haploid population. Mol Breed 37:1–10. https://doi.org/10.1007/s11032-017-0706-9
Singh AK, Krishnan SG, Vinod KK, Ellur RK, Bollinedi H, Bhowmick PK, Nagarajan M (2019) Precision breeding with genomic tools: a decade long journey of molecular breeding in rice. Indian J Genet Plant Breed 79(Sup-01):181–191.
Snape JW, Simpson E (1986) The utilisation of doubled haploid lines in quantitative genetics. Bulletin de la Société Botanique de France. Actualités Botaniques 133(4):59–66. https://doi.org/10.1080/01811789.1986.10826799
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Bio Evo 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Thompson KF (1972) Oil-seed rape. Reports of the plant breeding institute. Cambridge University Press, Cambridge, pp 94–96
Wang X (2001) Plant phospholipases. Annu Rev Plant Biol 52(1):211–231. https://doi.org/10.1146/annurev.arplant.52.1.211
Wang S, Ouyang K (2022) Rapid creation of CENH3-mediated haploid induction lines using a cytosine base editor (CBE). Plant Biol 25(1):226–230. https://doi.org/10.1111/plb.13482
Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019a) Development of a haploid-inducer mediated genome editing system for accelerating maize breeding. Mol Plant 12(4):597–602. https://doi.org/10.1016/j.molp.2019.03.006
Wang C, Liu Q, Shen Y, Hua Y, Wang J, Lin J, Wu M, Sun T, Cheng Z, Mercier R, Wang K (2019b) Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat Biotechnol 37(3):283–286. https://doi.org/10.1038/s41587-018-0003-0
Wang J, Cao Y, Wang K, Liu C (2022a) Development of multiple-heading-date mtl haploid inducer lines in rice. Agriculture 12(6):806. https://doi.org/10.3390/agriculture12060806
Wang N, Xia X, Jiang T, Li L, Zhang P, Niu L, Cheng H, Wang K, Lin H (2022b) In planta haploid induction by genome editing of DMP in the model legume Medicago truncatula. Plant Biotechnol J 20(1):22–24. https://doi.org/10.1111/pbi.13740
Wang N, Gent JI, Dawe RK (2021) Haploid induction by a maize CENH3 null mutant. Sci Adv 7(4): eabe2299. https://doi.org/10.1126/sciadv.abe2299
Watts A, Kumar V, Raipuria RK, Bhattacharya RC (2018) In vivo haploid production in crop plants: methods and challenges. Plant Mol Biol Rep 36(5):685–694. https://doi.org/10.1007/s11105-018-1132-9
Xie E, Li Y, Tang D, Lv Y, Shen Y, Cheng Z (2019) A strategy for generating rice apomixis by gene editing. J Integr Plant Biol 61(8):911–916. https://doi.org/10.1111/jipb.12785
Yao L, Zhang Y, Liu C, Liu Y, Wang Y, Liang D, Liu J, Sahoo G, Kelliher T (2018) OsMATL mutation induces haploid seed formation in indica rice. Nat Plants 4(8):530–533. https://doi.org/10.1038/s41477-018-0193-y
Yuan J, Guo X, Hu J, Lv Z, Han F (2015) Characterization of two CENH3 genes and their roles in wheat evolution. New Phytol 206(2):839–851. https://doi.org/10.1111/nph.13235
Zhong Y, Liu C, Qi X, Jiao Y, Wang D, Wang Y, Chen S (2019) Mutation of ZmDMP enhances haploid induction in maize. Nat Plants 5(6):575–580. https://doi.org/10.1038/s41477-019-0443-7
Zhong Y, Chen B, Li M, Wang D, Jiao Y, Qi X, Wang M, Liu Z, Chen C, Wang Y, Chen M (2020) A DMP-triggered in vivo maternal haploid induction system in the dicotyledonous Arabidopsis. Nat Plants 6(5):466–472. https://doi.org/10.1038/s41477-020-0658-7
Zhong Y, Chen B, Wang D, Zhu X, Li M, Zhang J, Chen M, Wang M, Riksen T, Liu J, Qi X (2022) In vivo maternal haploid induction in tomato. Plant Biotechnol J 20(2):250–252. https://doi.org/10.1111/pbi.13755
Zhu S, Wang X, Chen W, Yao J, Li Y, Fang S, Lv Y, Li X, Pan J, Liu C, Li Q (2021) Cotton DMP gene family: characterization, evolution, and expression profiles during development and stress. Int J Biol Macromol 183:1257–1269. https://doi.org/10.1016/j.ijbiomac.2021.05.023
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The financial support was provided by the Department of Biotechnology, India, under project number BT/GET/119/SP25803/2018 for carrying out this research.
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DB and LG conceived the idea, designed, and supervised the study; LG, MK, MM, DP, and SK carried out all the in silico analysis; LG wrote the first draft of the manuscript; DB, KAM, and LG edited and wrote the final version of manuscript. All authors read and approved the final manuscript.
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Goyal, L., Kaur, M., Mandal, M. et al. Potential gene editing targets for developing haploid inducer stocks in rice and wheat with high haploid induction frequency. 3 Biotech 14, 14 (2024). https://doi.org/10.1007/s13205-023-03857-9
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DOI: https://doi.org/10.1007/s13205-023-03857-9