{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T23:26:32Z","timestamp":1790724392921,"version":"4.1.0"},"reference-count":116,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T00:00:00Z","timestamp":1672876800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Major Project of Hubei Hongshan Laboratory","award":["2022hszd017"],"award-info":[{"award-number":["2022hszd017"]}]},{"name":"Major Project of Hubei Hongshan Laboratory","award":["2022CFA071"],"award-info":[{"award-number":["2022CFA071"]}]},{"name":"Major Project of Hubei Hongshan Laboratory","award":["31970340"],"award-info":[{"award-number":["31970340"]}]},{"name":"Science and Technology Department of Hubei Province","award":["2022hszd017"],"award-info":[{"award-number":["2022hszd017"]}]},{"name":"Science and Technology Department of Hubei Province","award":["2022CFA071"],"award-info":[{"award-number":["2022CFA071"]}]},{"name":"Science and Technology Department of Hubei Province","award":["31970340"],"award-info":[{"award-number":["31970340"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2022hszd017"],"award-info":[{"award-number":["2022hszd017"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2022CFA071"],"award-info":[{"award-number":["2022CFA071"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31970340"],"award-info":[{"award-number":["31970340"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Although zygotic embryogenesis is usually studied in the field of seed biology, great attention has been paid to the methods used to generate haploid embryos due to their applications in crop breeding. These mainly include two methods for haploid embryogenesis: in vitro microspore embryogenesis and in vivo haploid embryogenesis. Although microspore culture systems and maize haploid induction systems were discovered in the 1960s, little is known about the molecular mechanisms underlying haploid formation. In recent years, major breakthroughs have been made in in vivo haploid induction systems, and several key factors, such as the matrilineal (MTL), baby boom (BBM), domain of unknown function 679 membrane protein (DMP), and egg cell-specific (ECS) that trigger in vivo haploid embryo production in both the crops and Arabidopsis models have been identified. The discovery of these haploid inducers indicates that haploid embryogenesis is highly related to gamete development, fertilization, and genome stability in ealry embryos. Here, based on recent efforts to identify key players in haploid embryogenesis and to understand its molecular mechanisms, we summarize the different paths to haploid embryogenesis, and we discuss the mechanisms of haploid generation and its potential applications in crop breeding. Although these haploid-inducing factors could assist egg cells in bypassing fertilization to initiate embryogenesis or trigger genome elimination in zygotes after fertilization to form haploid embryos, the fertilization of central cells to form endosperms is a prerequisite step for haploid formation. Deciphering the molecular and cellular mechanisms for haploid embryogenesis, increasing the haploid induction efficiency, and establishing haploid induction systems in other crops are critical for promoting the application of haploid technology in crop breeding, and these should be addressed in further studies.<\/jats:p>","DOI":"10.3390\/plants12020243","type":"journal-article","created":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T04:12:56Z","timestamp":1672891976000},"page":"243","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["The Roads to Haploid Embryogenesis"],"prefix":"10.3390","volume":"12","author":[{"given":"Kun","family":"Shen","sequence":"first","affiliation":[{"name":"State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengxue","family":"Qu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1904-8955","authenticated-orcid":false,"given":"Peng","family":"Zhao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1007\/s11032-021-01204-5","article-title":"Haploid induction and its application in maize breeding","volume":"41","author":"Meng","year":"2021","journal-title":"Mol. Breed."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1007\/s001220100602","article-title":"Inheritance of microspore embryogenic ability in Brassica crops","volume":"103","author":"Zhang","year":"2001","journal-title":"Theor. Appl. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1007\/s11738-005-0070-y","article-title":"Cell architecture during gametophytic and embryogenic microspore development in Brassica napus L.","volume":"27","author":"Satpute","year":"2005","journal-title":"Acta Physiol. Plant."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1111\/j.1399-3054.2006.00675.x","article-title":"Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis","volume":"127","author":"Shariatpanahi","year":"2006","journal-title":"Physiol. Plant."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2639","DOI":"10.1093\/jxb\/erl027","article-title":"The role of arabinogalactan proteins binding to Yariv reagents in the initiation, cell developmental fate, and maintenance of microspore embryogenesis in Brassica napus L. cv. Topas","volume":"57","author":"Tang","year":"2006","journal-title":"J. Exp. Bot."},{"key":"ref_6","first-page":"283","article-title":"Anther culture for haploid and doubled haploid production","volume":"104","year":"2010","journal-title":"Plant Cell Tissue Organ Cult."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Prem, D., Solis, M.T., Barany, I., Rodriguez-Sanz, H., Risueno, M.C., and Testillano, P.S. (2012). A new microspore embryogenesis system under low temperature which mimics zygotic embryogenesis initials, expresses auxin and efficiently regenerates doubled-haploid plants in Brassica napus. BMC Plant Biol., 12.","DOI":"10.1186\/1471-2229-12-127"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/s10681-017-1879-3","article-title":"Development and characterization of an eggplant (Solanum melongena) doubled haploid population and a doubled haploid line with high androgenic response","volume":"213","year":"2017","journal-title":"Euphytica"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1007\/s00412-004-0279-3","article-title":"Spontaneous chromosome doubling results from nuclear fusion during in vitro maize induced microspore embryogenesis","volume":"112","author":"Testillano","year":"2004","journal-title":"Chromosoma"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1595","DOI":"10.1016\/j.jplph.2006.11.012","article-title":"Antimitotic agents increase the production of doubled-haploid embryos from cork oak anther culture","volume":"164","author":"Pintos","year":"2007","journal-title":"J. Plant Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1093\/jxb\/ers327","article-title":"Exine dehiscing induces rape microspore polarity, which results in different daughter cell fate and fixes the apical-basal axis of the embryo","volume":"64","author":"Tang","year":"2013","journal-title":"J. Exp. Bot."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2965","DOI":"10.1093\/jxb\/ery464","article-title":"Microspore embryogenesis: Targeting the determinant factors of stress-induced cell reprogramming for crop improvement","volume":"70","author":"Testillano","year":"2019","journal-title":"J. Exp. Bot."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1105\/tpc.113.116491","article-title":"The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte","volume":"26","author":"Li","year":"2014","journal-title":"Plant Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.scienta.2016.05.001","article-title":"Effects of histone deacetylase inhibitors on microspore embryogenesis and plant regeneration in Pakchoi (Brassica rapa ssp. chinensis L.)","volume":"209","author":"Zhang","year":"2016","journal-title":"Sci. Hortic."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1701","DOI":"10.1007\/s00299-017-2183-3","article-title":"Trichostatin A increases embryo and green plant regeneration in wheat","volume":"36","author":"Jiang","year":"2017","journal-title":"Plant Cell Rep."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Castillo, A.M., Valero-Rubira, I., Burrell, M.A., Allue, S., Costar, M.A., and Valles, M.P. (2020). Trichostatin A Affects Developmental Reprogramming of Bread Wheat Microspores towards an Embryogenic Route. Plants, 9.","DOI":"10.3390\/plants9111442"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/s00497-017-0302-5","article-title":"Dynamics of post-translationally modified histones during barley pollen embryogenesis in the presence or absence of the epi-drug trichostatin A","volume":"30","author":"Pandey","year":"2017","journal-title":"Plant Reprod."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"110189","DOI":"10.1016\/j.plantsci.2019.110189","article-title":"Chemically-induced DNA de-methylation alters the effectiveness of microspore embryogenesis in triticale","volume":"287","author":"Nowicka","year":"2019","journal-title":"Plant Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.3389\/fpls.2017.01161","article-title":"Inhibition of Histone H3K9 Methylation by BIX-01294 Promotes Stress-Induced Microspore Totipotency and Enhances Embryogenesis Initiation","volume":"8","author":"Berenguer","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"6431","DOI":"10.1093\/jxb\/ers298","article-title":"DNA methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis","volume":"63","author":"Solis","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1016\/j.biotechadv.2015.07.001","article-title":"Haploids: Constraints and opportunities in plant breeding","volume":"33","author":"Dwivedi","year":"2015","journal-title":"Biotechnol. Adv."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"751230","DOI":"10.3389\/fpls.2021.751230","article-title":"Androgenesis-Based Doubled Haploidy: Past, Present, and Future Perspectives","volume":"12","author":"Hale","year":"2021","journal-title":"Front. Plant Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2180","DOI":"10.1080\/15548627.2020.1719722","article-title":"Autophagy-mediated compartmental cytoplasmic deletion is essential for tobacco pollen germination and male fertility","volume":"16","author":"Zhao","year":"2020","journal-title":"Autophagy"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Yan, H., Zhuang, M., Xu, X., Li, S., Yang, M., Li, N., Du, X., Hu, K., Peng, X., and Huang, W. (2022). Autophagy and its mediated mitochondrial quality control maintain pollen tube growth and male fertility in Arabidopsis. Autophagy, 1\u201316.","DOI":"10.1080\/15548627.2022.2095838"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3061","DOI":"10.1093\/jxb\/ert151","article-title":"Novel features of Brassica napus embryogenic microspores revealed by high pressure freezing and freeze substitution: Evidence for massive autophagy and excretion-based cytoplasmic cleaning","volume":"64","year":"2013","journal-title":"J. Exp. Bot."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1093\/jxb\/erx455","article-title":"Autophagy is activated and involved in cell death with participation of cathepsins during stress-induced microspore embryogenesis in barley","volume":"69","author":"Barany","year":"2018","journal-title":"J. Exp. Bot."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2097","DOI":"10.1093\/pcp\/pcaa128","article-title":"Suppression of Metacaspase- and Autophagy-Dependent Cell Death Improves Stress-Induced Microspore Embryogenesis in Brassica napus","volume":"61","author":"Berenguer","year":"2021","journal-title":"Plant Cell Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2007","DOI":"10.1093\/jxb\/err400","article-title":"NO, ROS, and cell death associated with caspase-like activity increase in stress-induced microspore embryogenesis of barley","volume":"63","author":"Barany","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1279","DOI":"10.1007\/s00299-009-0730-2","article-title":"Stress-related variation in antioxidative enzymes activity and cell metabolism efficiency associated with embryogenesis induction in isolated microspore culture of triticale (x Triticosecale Wittm.)","volume":"28","author":"Zur","year":"2009","journal-title":"Plant Cell Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"6620","DOI":"10.1128\/MCB.24.15.6620-6630.2004","article-title":"Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae","volume":"24","author":"Wieland","year":"2004","journal-title":"Mol. Cell. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1105\/tpc.010425","article-title":"Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant","volume":"14","author":"Talbert","year":"2002","journal-title":"Plant Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1111\/j.1365-313X.2011.04664.x","article-title":"Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation","volume":"68","author":"Lermontova","year":"2011","journal-title":"Plant J."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Ravi, M., Shibata, F., Ramahi, J.S., Nagaki, K., Chen, C., Murata, M., and Chan, S.W. (2011). Meiosis-specific loading of the centromere-specific histone CENH3 in Arabidopsis thaliana. PLoS Genet., 7.","DOI":"10.1371\/journal.pgen.1002121"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"E498","DOI":"10.1073\/pnas.1103190108","article-title":"Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids","volume":"108","author":"Sanei","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/j.devcel.2014.08.016","article-title":"The centromere: Chromatin foundation for the kinetochore machinery","volume":"30","author":"Fukagawa","year":"2014","journal-title":"Dev. Cell"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1146\/annurev-arplant-043014-114714","article-title":"Haploidization via Chromosome Elimination: Means and Mechanisms","volume":"67","author":"Ishii","year":"2016","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.pbi.2017.03.003","article-title":"Plant centromeres","volume":"36","author":"Comai","year":"2017","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.molp.2017.12.009","article-title":"Centromere Size and Its Relationship to Haploid Formation in Plants","volume":"11","author":"Wang","year":"2018","journal-title":"Mol. Plant"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1111\/pbi.13365","article-title":"A variety of changes, including CRISPR\/Cas9-mediated deletions, in CENH3 lead to haploid induction on outcrossing","volume":"18","author":"Kuppu","year":"2020","journal-title":"Plant Biotechnol. J."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1534\/genetics.110.120337","article-title":"The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana","volume":"186","author":"Ravi","year":"2010","journal-title":"Genetics"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Maheshwari, S., Tan, E.H., West, A., Franklin, F.C., Comai, L., and Chan, S.W. (2015). Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1004970"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"11211","DOI":"10.1073\/pnas.1504333112","article-title":"Point mutation impairs centromeric CENH3 loading and induces haploid plants","volume":"112","author":"Ishii","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Kuppu, S., Tan, E.H., Nguyen, H., Rodgers, A., Comai, L., Chan, S.W., and Britt, A.B. (2015). Point Mutations in Centromeric Histone Induce Post-zygotic Incompatibility and Uniparental Inheritance. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005494"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"357","DOI":"10.3389\/fpls.2016.00357","article-title":"Cenh3: An Emerging Player in Haploid Induction Technology","volume":"7","author":"Britt","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1007\/s13562-016-0368-4","article-title":"Centromeric histone H3 protein: From basic study to plant breeding applications","volume":"25","author":"Watts","year":"2016","journal-title":"J. Plant Biochem. Biotechnol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1361","DOI":"10.1111\/pbi.12805","article-title":"Novel technologies in doubled haploid line development","volume":"15","author":"Ren","year":"2017","journal-title":"Plant Biotechnol. J."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.ceb.2018.01.011","article-title":"The cellular mechanisms and consequences of centromere drive","volume":"52","author":"Kursel","year":"2018","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/j.tig.2019.07.005","article-title":"Haploid Induction and Genome Instability","volume":"35","author":"Comai","year":"2019","journal-title":"Trends Genet."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1007\/s00122-018-3261-9","article-title":"State-of-the-art and novel developments of in vivo haploid technologies","volume":"132","author":"Kalinowska","year":"2019","journal-title":"Theor. Appl. Genet."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/s13007-019-0429-5","article-title":"Centromere histone H3- and phospholipase-mediated haploid induction in plants","volume":"15","author":"Wang","year":"2019","journal-title":"Plant Methods"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-0716-1331-3_1","article-title":"Centromere engineering as an emerging tool for haploid plant production: Advances and challenges","volume":"2289","year":"2021","journal-title":"Doubled Haploid Technol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2051","DOI":"10.1111\/pbi.13875","article-title":"Centromeres: From chromosome biology to biotechnology applications and synthetic genomes in plants","volume":"20","author":"Zhou","year":"2022","journal-title":"Plant Biotechnol. J."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1038\/nature08842","article-title":"Haploid plants produced by centromere-mediated genome elimination","volume":"464","author":"Ravi","year":"2010","journal-title":"Nature"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"eabk1151","DOI":"10.1126\/sciadv.abk1151","article-title":"Epigenetically mismatched parental centromeres trigger genome elimination in hybrids","volume":"7","author":"Marimuthu","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"eabe2299","DOI":"10.1126\/sciadv.abe2299","article-title":"Haploid induction by a maize cenh3 null mutant","volume":"7","author":"Wang","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/nature10802","article-title":"DNA breaks and chromosome pulverization from errors in mitosis","volume":"482","author":"Crasta","year":"2012","journal-title":"Nature"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1086\/282098","article-title":"A Line of Maize with High Haploid Frequency","volume":"93","author":"Coe","year":"1959","journal-title":"Am. Nat."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1038\/nature20827","article-title":"MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction","volume":"542","author":"Kelliher","year":"2017","journal-title":"Nature"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.molp.2017.01.011","article-title":"A 4-bp Insertion at ZmPLA1 Encoding a Putative Phospholipase A Generates Haploid Induction in Maize","volume":"10","author":"Liu","year":"2017","journal-title":"Mol. Plant"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"707","DOI":"10.15252\/embj.201796603","article-title":"Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize","volume":"36","author":"Gilles","year":"2017","journal-title":"EMBO J."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/978-1-61779-600-5_8","article-title":"Plant Phospholipases: An Overview","volume":"861","author":"Wang","year":"2012","journal-title":"Methods Mol. Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/978-1-4939-8672-9_3","article-title":"Phospholipases: An overview","volume":"1835","author":"Aloulou","year":"2018","journal-title":"Lipases Phospholipases"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"101158","DOI":"10.1016\/j.plipres.2022.101158","article-title":"The functions of phospholipases and their hydrolysis products in plant growth, development and stress responses","volume":"86","author":"Ali","year":"2022","journal-title":"Prog. Lipid Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"e202010077","DOI":"10.1083\/jcb.202010077","article-title":"Lipid anchoring and electrostatic interactions target NOT-LIKE-DAD to pollen endo-plasma membrane","volume":"220","author":"Gilles","year":"2021","journal-title":"J. Cell Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1038\/s41477-019-0443-7","article-title":"Mutation of ZmDMP enhances haploid induction in maize","volume":"5","author":"Zhong","year":"2019","journal-title":"Nat. Plants"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1111\/jipb.13270","article-title":"An in planta haploid induction system in Brassica napus","volume":"64","author":"Li","year":"2022","journal-title":"J. Integr. Plant Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1111\/jipb.13244","article-title":"Establishment of a dmp based maternal haploid induction system for polyploid Brassica napus and Nicotiana tabacum","volume":"64","author":"Zhong","year":"2022","journal-title":"J. Integr. Plant Biol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"2242","DOI":"10.1111\/pbi.13934","article-title":"In vivo maternal haploid induction based on genome editing of DMP in Brassica oleracea","volume":"20","author":"Zhao","year":"2022","journal-title":"Plant Biotechnol. J."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1111\/pbi.13740","article-title":"In planta haploid induction by genome editing of DMP in the model legume Medicago truncatula","volume":"20","author":"Wang","year":"2022","journal-title":"Plant Biotechnol. J."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1007\/s00425-022-03877-4","article-title":"Haploid induction in allotetraploid tobacco using DMPs mutation","volume":"255","author":"Zhang","year":"2022","journal-title":"Planta"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1111\/pbi.13755","article-title":"In vivo maternal haploid induction in tomato","volume":"20","author":"Zhong","year":"2022","journal-title":"Plant Biotechnol. J."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/s42994-022-00080-7","article-title":"Construction of homozygous diploid potato through maternal haploid induction","volume":"3","author":"Zhang","year":"2022","journal-title":"aBIOTECH"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1038\/s41477-021-01037-2","article-title":"Loss-of-function alleles of ZmPLD3 cause haploid induction in maize","volume":"7","author":"Li","year":"2021","journal-title":"Nat. Plants"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1016\/j.molp.2022.04.001","article-title":"A reactive oxygen species burst causes haploid induction in maize","volume":"15","author":"Jiang","year":"2022","journal-title":"Mol. Plant"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1038\/s41586-021-03387-5","article-title":"Fertilized egg cells secrete endopeptidases to avoid polytubey","volume":"592","author":"Yu","year":"2021","journal-title":"Nature"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Mao, Y., Nakel, T., Serbes, I.E., Tekleyohans, D.G., Joshi, S., Baum, T., and Gro\u00df-Hardt, R. (2022). ECS1 and ECS2 regulate polyspermy and suppress the formation of haploid plants by promoting double fertilization. BioRxiv.","DOI":"10.1101\/2022.01.20.476184"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Zhang, X., Shi, C., Li, s., Zhang, B., Dresselhaus, T., and Sun, M.-x. (2022). A female in vivo haploid-induction system via mutagenesis of egg cell-specific peptidases. Res. Sq.","DOI":"10.21203\/rs.3.rs-1340747\/v1"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1104\/pp.113.223982","article-title":"Fertilization and uniparental chromosome elimination during crosses with maize haploid inducers","volume":"163","author":"Zhao","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1038\/s41587-019-0038-x","article-title":"One-step genome editing of elite crop germplasm during haploid induction","volume":"37","author":"Kelliher","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2405","DOI":"10.1111\/nph.17963","article-title":"Matrilineal empowers wheat pollen with haploid induction potency by triggering postmitosis reactive oxygen species activity","volume":"233","author":"Sun","year":"2022","journal-title":"New Phytol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1038\/s41467-017-00969-8","article-title":"Single nucleus sequencing reveals spermatid chromosome fragmentation as a possible cause of maize haploid induction","volume":"8","author":"Li","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1093\/jxb\/ern318","article-title":"Specific functions of individual class III peroxidase genes","volume":"60","author":"Cosio","year":"2009","journal-title":"J. Exp. Bot."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1007\/s00253-002-1157-7","article-title":"Molecular biology and application of plant peroxidase genes","volume":"60","author":"Yoshida","year":"2003","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1016\/j.molp.2022.05.010","article-title":"Highly reactive chemicals meet haploidization","volume":"15","author":"Ruban","year":"2022","journal-title":"Mol. Plant"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1737","DOI":"10.1105\/tpc.001941","article-title":"Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth","volume":"14","author":"Boutilier","year":"2002","journal-title":"Plant Cell"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1007\/s11103-010-9674-8","article-title":"Control of somatic embryogenesis and embryo development by AP2 transcription factors","volume":"74","author":"Schnell","year":"2010","journal-title":"Plant Mol. Biol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/s10725-012-9676-4","article-title":"Identification of BABY BOOM and LEAFY COTYLEDON genes in sweet pepper (Capsicum annuum L.) genome by their partial gene sequences","volume":"67","author":"Irikova","year":"2012","journal-title":"Plant Growth Regul."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Salvo, S.A., Hirsch, C.N., Buell, C.R., Kaeppler, S.M., and Kaeppler, H.F. (2014). Whole transcriptome profiling of maize during early somatic embryogenesis reveals altered expression of stress factors and embryogenesis-related genes. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0111407"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Florez, S.L., Erwin, R.L., Maximova, S.N., Guiltinan, M.J., and Curtis, W.R. (2015). Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol., 15.","DOI":"10.1186\/s12870-015-0479-4"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1849","DOI":"10.1007\/s00299-015-1832-7","article-title":"Steroid-inducible BABY BOOM system for development of fertile Arabidopsis thaliana plants after prolonged tissue culture","volume":"34","author":"Lutz","year":"2015","journal-title":"Plant Cell Rep."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1104\/pp.17.00232","article-title":"The BABY BOOM Transcription Factor Activates the LEC1-ABI3-FUS3-LEC2 Network to Induce Somatic Embryogenesis","volume":"175","author":"Horstman","year":"2017","journal-title":"Plant Physiol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1467","DOI":"10.1007\/s10529-018-2613-5","article-title":"BABY BOOM (BBM): A candidate transcription factor gene in plant biotechnology","volume":"40","author":"Jha","year":"2018","journal-title":"Biotechnol. Lett."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"11205","DOI":"10.1073\/pnas.1505856112","article-title":"A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant","volume":"112","author":"Conner","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/s00497-017-0298-x","article-title":"Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes","volume":"30","author":"Conner","year":"2017","journal-title":"Plant Reprod."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1111\/tpj.13479","article-title":"A fern AINTEGUMENTA gene mirrors BABY BOOM in promoting apogamy in Ceratopteris richardii","volume":"90","author":"Bui","year":"2017","journal-title":"Plant J."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1038\/s41586-018-0785-8","article-title":"A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds","volume":"565","author":"Khanday","year":"2019","journal-title":"Nature"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Zhang, Z., Conner, J., Guo, Y., and Ozias-Akins, P. (2020). Haploidy in Tobacco Induced by PsASGR-BBML Transgenes via Parthenogenesis. Genes, 11.","DOI":"10.3390\/genes11091072"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"863908","DOI":"10.3389\/fpls.2022.863908","article-title":"Phylogenetically Distant BABY BOOM Genes from Setaria italica Induce Parthenogenesis in Rice","volume":"13","author":"Chahal","year":"2022","journal-title":"Front. Plant Sci."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"e2201761119","DOI":"10.1073\/pnas.2201761119","article-title":"BABY BOOM regulates early embryo and endosperm development","volume":"119","author":"Chen","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1038\/s41588-021-00984-y","article-title":"A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce","volume":"54","author":"Underwood","year":"2022","journal-title":"Nat. Genet."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1038\/s41477-018-0193-y","article-title":"OsMATL mutation induces haploid seed formation in indica rice","volume":"4","author":"Yao","year":"2018","journal-title":"Nat. Plants"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1038\/s41587-018-0003-0","article-title":"Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes","volume":"37","author":"Wang","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1111\/pbi.13218","article-title":"Extension of the in vivo haploid induction system from diploid maize to hexaploid wheat","volume":"18","author":"Liu","year":"2020","journal-title":"Plant Biotechnol. J."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1111\/pbi.13584","article-title":"Establishing in planta haploid inducer line by edited SiMTL in foxtail millet (Setaria italica)","volume":"19","author":"Cheng","year":"2021","journal-title":"Plant Biotechnol. J."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1038\/s41477-020-0658-7","article-title":"A DMP-triggered in vivo maternal haploid induction system in the dicotyledonous Arabidopsis","volume":"6","author":"Zhong","year":"2020","journal-title":"Nat. Plants"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"5334","DOI":"10.1038\/ncomms6334","article-title":"A haploid genetics toolbox for Arabidopsis thaliana","volume":"5","author":"Ravi","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"414","DOI":"10.3389\/fpls.2016.00414","article-title":"Maternal Haploids Are Preferentially Induced by CENH3-tailswap Transgenic Complementation in Maize","volume":"7","author":"Kelliher","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.molp.2019.03.006","article-title":"Development of a Haploid-Inducer Mediated Genome Editing System for Accelerating Maize Breeding","volume":"12","author":"Wang","year":"2019","journal-title":"Mol. Plant"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1111\/tpj.14606","article-title":"The deposition of CENH3 in maize is stringently regulated","volume":"102","author":"Feng","year":"2020","journal-title":"Plant J."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1038\/s41477-020-0664-9","article-title":"Puzzling out plant reproduction by haploid induction for innovations in plant breeding","volume":"6","author":"Jacquier","year":"2020","journal-title":"Nat. Plants"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.tig.2019.12.006","article-title":"Clonal Reproduction through Seeds in Sight for Crops","volume":"36","author":"Conner","year":"2020","journal-title":"Trends Genet."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1146\/annurev-arplant-102720-013958","article-title":"Engineering Apomixis: Clonal Seeds Approaching the Fields","volume":"73","author":"Underwood","year":"2022","journal-title":"Annu. Rev. Plant. Biol."},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"d\u2019Erfurth, I., Jolivet, S., Froger, N., Catrice, O., Novatchkova, M., and Mercier, R. (2009). Turning meiosis into mitosis. PLoS Biol., 7.","DOI":"10.1371\/journal.pbio.1000124"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"1242","DOI":"10.1038\/cr.2016.117","article-title":"Turning rice meiosis into mitosis","volume":"26","author":"Mieulet","year":"2016","journal-title":"Cell Res."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1126\/science.1199682","article-title":"Synthetic clonal reproduction through seeds","volume":"331","author":"Marimuthu","year":"2011","journal-title":"Science"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"100470","DOI":"10.1016\/j.xplc.2022.100470","article-title":"Synthetic apomixis enables stable transgenerational transmission of heterotic phenotypes in hybrid rice","volume":"4","author":"Liu","year":"2022","journal-title":"Plant Commun."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/2\/243\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T17:59:36Z","timestamp":1760119176000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/2\/243"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,5]]},"references-count":116,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["plants12020243"],"URL":"https:\/\/doi.org\/10.3390\/plants12020243","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,5]]}}}