Skip to main content
Log in

CENH3 mediated haploid induction: application and future perspectives in crop plants

  • Review Article
  • Published:
Horticulture, Environment, and Biotechnology Aims and scope Submit manuscript

Abstract

True homozygous pure lines are required for the development of new crop varieties. In conventional as well as molecular breeding strategies, it typically takes 7–9 generations to accomplish the appropriate level of homozygosity. On the contrary, haploids can have their chromosomes doubled in a single generation to create a true-breeding lineage. Over the period, researchers have developed several methods for haploids and doubled haploid induction, but these methods are only applicable to specific crop types. The discovery of the centromere-specific histone 3 variant (CENH3) and its manipulation is proving to be the most potent technique for haploid development. Recent advancements in this technology have shown that non-transgenic changes to CENH3 can also induce haploids. Point mutations in CENH3 that can be induced by chemical agents may lead to haploid induction when crossed with wild-type CENH3 plants. These plants with the CENH3 mutation are fully fertile when selfed, develop properly, and can be found in already-existing collections of mutagenized plants. The current review encompasses the recent studies undertaken to utilize the CENH3 manipulations strategy to develop various haploid plant crops with increased success rates. This review paper will provide a better insight into understanding the detailed mechanism of the CENH3-induced haploid induction process and help investigate the areas that need to be further explored.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

(source: Sanei et al. 2011). (A) Cross between H. vulgare and H. bilbosum (B) All parental CENH3 are transcriptionally active; CENH3 (red) loaded on the centromeres of H. vulgare, but CENH3 (blue) not loaded on H. bulbosum (C) Centromere inactivity of anaphase chromosomes of H. bulbosum lag and thus degrades and haploid H. vulgare develops

Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anandhan S, Chavan AA, Gopal J, Mote SR, Shelke PV, Lawande KE (2014) Variation in gynogenic potential for haploid induction in Indian short-day onions. Indian J Genet Plant Breed 74(4):526–528

    Google Scholar 

  • Arjun H, Rajesh B, Goud SV, Lokesha S, Kumar PS (2020) Effect of pre and post culture temperature treatments on direct microspore embryogenesis in Indian Chilli pepper (Capsicum annuum L). Plant Cell Biotechnol Mol Biol 21(1–2):49–58

    Google Scholar 

  • Assani A, Bakry F, Kerbellec F, Haicour R, Wenzel G, Foroughi-Wehr (2003) Production of haploids from anther culture of banana [Musa balbisiana (BB)]. Plant Cell Rep 21(6):511–516

    PubMed  Google Scholar 

  • Benega R, Isidrón M, Arias E, Cisneros A, Martínez J, Companioni L, Borroto C (1995) Plant regeneration from pineapple ovules (Ananas comosus (L.) Merr.). In: II International Pineapple Symposium 425, pp 247–250

  • Benega R, Cisneros A, Martinez J, Arias E, Yabor L, Isidron M, Castillo E, Fernandez J (1997) Pollen-gamma irradiation on pineapple and pollination using irradiated pollen; irradiacion gamma de Polen De Pina. Fecundacion con pollen irradiado. Nucleus 24:12–14

    Google Scholar 

  • Britt AB, Kuppu S (2016) Cenh3: an emerging player in haploid induction technology. Front Plant Sci 7:357

    PubMed  PubMed Central  Google Scholar 

  • Camp OPD, Rik HM (2017) Method for the production of haploid and subsequent doubled haploid plants. patent no. WO 2017/200386 A1

  • Comai L, Tan EH (2019) Haploid induction and genome instability. Trends Genet 35(11):791–803

    PubMed  Google Scholar 

  • Diao WP, Jia YY, Song H, Zhang XQ, Lou QF, Chen JF (2009) Efficient embryo induction in cucumber ovary culture and homozygous identification of the regenetants using SSR markers. Scientia Hort 119(3):246–251

    Google Scholar 

  • Dunemann F, Schrader O, Budahn H, Houben A (2014) Characterization of centromeric histone H3 (CENH3) variants in cultivated and wild carrots (Daucus Sp). PLoS ONE 9(6):e98504

    PubMed  PubMed Central  Google Scholar 

  • Esen A, Soost RK (1971) Unexpected triploids in Citrus: their origin, identification, and possible use. J Hered 62(6):329–333

    Google Scholar 

  • Evtushenko EV, Elisafenko EA, Gatzkaya SS, Lipikhina YA, Houben A, Vershinin AV (2017) Conserved molecular structure of the centromeric histone CENH3 in Secale and its phylogenetic relationships. Sci Rep 7(1):17628

    PubMed  PubMed Central  Google Scholar 

  • Fei KW, Xue, GR JC-knykohSas (1981) Induction of haploid plantlets by anther culture in vitro in apple cv. Delic Sci Agric Sin 4:41–44

    Google Scholar 

  • Finch RA (1983) Tissue-specific elimination of alternative whole parental genomes in one barley hybrid. Chromosoma 88(5):386–393

    Google Scholar 

  • Heckmann S, Lermontova I, Berckmans B, De Veylder L, Bäumlein H, Schubert I (2011) The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J 68(4):646–656

    PubMed  Google Scholar 

  • Hirsch CD, Wu Y, Yan H, Jiang J (2009) Lineage-specific adaptive evolution of the centromeric protein CENH3 in diploid and allotetraploid Oryza species. Mol Bio Evol 26(12):2877–2885

    Google Scholar 

  • Ingouff M, Rademacher S, Holec S, Šoljić L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20(23):2137–2143

    PubMed  Google Scholar 

  • Ishii T, Karimi-Ashtiyani R, Houben A (2016) Haploidization via chromosome elimination: means and mechanisms. Annu Rev Plant Biol 67:421–438

    PubMed  Google Scholar 

  • Iwata A, Tek AL, Richard MM, Abernathy B, Fonseca A, Schmutz J, Chen NW, Thareau V, Magdelenat G et al (2013) Identification and characterization of functional centromeres of the common bean. Plant J 76(1):47–60

    PubMed  Google Scholar 

  • Kadota M, Niimi Y (2004) Production of triploid plants of Japanese pear (Pyrus pyrifolia Nakai) by anther culture. Euphytica 138(2):141–147

    Google Scholar 

  • Kara Z, Yazar K, Ekinci H (2018) Somatic embryogenesis and plant regeneration from anther culture in grape cultivar’Ekşi Kara‘(Vitis vinifera L.). In: XXX International Horticultural Congress IHC2018: International Symposium on Viticulture: Primary Production and Processing 1276, pp 147–154

  • Karimi-Ashtiyani R, Ishii T, Niessen M, Stein N, Heckmann S, Gurushidze M, Banaei-Moghaddam AM, Fuchs J et al (2015) Point mutation impairs centromeric CENH3 loading and induces haploid plants. PNAS 112(36):11211–11216

    PubMed  PubMed Central  Google Scholar 

  • Kelliher T, Starr D, Wang W, McCuiston J, Zhong H, Nuccio ML, Martin B (2016) Maternal haploids are preferentially induced by CENH3-tailswap transgenic complementation in maize. Front Plant Sci 7:414

    PubMed  PubMed Central  Google Scholar 

  • Kiełkowska A, Adamus A (2010) In vitro culture of unfertilized ovules in carrot (Daucus carota L). PCTOC 102(3):309–319

    Google Scholar 

  • Kumar KR, Singh KP, Raju D, Bhatia R, Panwar S (2020) Maternal haploid induction in African marigold (Tagetes erecta L.) through in vitro culture of un-fertilized ovules. PCTOC 143(3):549–564

    Google Scholar 

  • Kundu M, Dubey A (2020) Effect of gamma ray irradiated pollen technique on seed development pattern in Citrus. ISGPB 80(04):450–458

    Google Scholar 

  • Kuppu S, Tan EH, Nguyen H, Rodgers A, Comai L, Chan SW, Britt AB (2015) Point mutations in centromeric histone induce post-zygotic incompatibility and uniparental inheritance. PloS Genet 11(9):e1005494

    PubMed  PubMed Central  Google Scholar 

  • Kuppu S, Ron M, Marimuthu MP, Li G, Huddleson A, Siddeek MH, Terry J, Buchner R, Shabek N, Comai, 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

    PubMed  PubMed Central  Google Scholar 

  • Li F, Cheng Y, Zhao X, Yu R, Li H, Wang L, Li S, Shan Q (2020) Haploid induction via unpollinated ovule culture in Gerbera hybrida. Sci Rep 10(1):1–9

    Google Scholar 

  • Lv J, Yu K, Wei J, Gui H, Liu C, Liang D, Wang Y, Zhou H, Carlin R, Rich R et al (2020) Generation of paternal haploids in wheat by genome editing of the centromeric histone CENH3. Nat Biotechnol 38(12):1397–1401

    PubMed  Google Scholar 

  • Maheshwari S, Tan EH, West A, Franklin FCH, Comai L, Chan SWL (2015) Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PloS Genet 11(1):e1004970

    PubMed  PubMed Central  Google Scholar 

  • Marimuthu MP, Maruthachalam R, Bondada R, Kuppu S, Tan EH, Britt A, Chan SW, Comai L (2021) Epigenetically mismatched parental centromeres trigger genome elimination in hybrids. Sci Adv 7(47):eabk1151

    PubMed  PubMed Central  Google Scholar 

  • Marin-Montes IM, Rodríguez-Pérez JE, Robledo-Paz A, de la Cruz-Torres E, Peña-Lomelí A, Sahagún-Castellanos J (2022) Haploid induction in Tomato (Solanum lycopersicum L.) via Gynogenesis. Plants (Basel) 11(12):1595

    PubMed  Google Scholar 

  • Meng D, Liu C, Chen S, Jin W (2021) Haploid induction and its application in maize breeding. Mol Plant Breed 41(3):1–9

    Google Scholar 

  • Meng D, Luo H, Dong Z, Huang W, Liu F, Li F, Chen S, Yu H, Jin W (2022) Overexpression of modified CENH3 in maize Stock6-derived inducer lines can effectively improve maternal haploid induction rates. Front Plant Sci 1053

  • Miao J, Frazier T, Huang L, Zhang X, Zhao B (2016) Identification and characterization of switchgrass histone H3 and CENH3 genes. Front Plant Sci 7:979

    PubMed  PubMed Central  Google Scholar 

  • Michellon R, Hugard J, Jonard RJCASPSD (1974) Sur l’isolément de colonies tissulaires de pêcher (Prunus persica Batsch., cultivars Dixired and Nectared IV) et d’amandier (Prunus amygdalus Stokes, Cultivar Ai) a partir d’anthères cultivées in vitro. C R Acad Sci Paris Série D 278:1719–1722

    Google Scholar 

  • Muiruri KS, Britt A, Amugune NO, Nguu EK, Chan S, Tripathi L (2017) Expressed centromere specific histone 3 (CENH3) variants in cultivated triploid and wild diploid bananas (Musa spp). Front Plant Sci 8:1034

    PubMed  PubMed Central  Google Scholar 

  • Nagaki K, Kashihara K, Murata M (2009) A centromeric DNA sequence colocalized with a centromere-specific histone H3 in Tobacco. Chromosoma 118(2):249–257

    PubMed  Google Scholar 

  • Nagaki K, Yamamoto M, Yamaji N, Mukai Y, Murata M (2012) Chromosome dynamics visualized with an anti-centromeric histone H3 antibody in Allium. PLoS ONE 7(12):e51315

    PubMed  PubMed Central  Google Scholar 

  • Neumann P, Navratilova A, Schroeder-Reiter E, Koblížková A, Steinbauerova V, Chocholova E, Novak P, Wanner G, Macas J (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PloS Genet 8(6):e1002777

    PubMed  PubMed Central  Google Scholar 

  • Niazian M, Shariatpanahi ME, Abdipour M, Oroojloo M (2019) Modeling callus induction and regeneration in an anther culture of tomato (Lycopersicon esculentum L.) using image processing and artificial neural network method. Protoplasma 256(5):1317–1332

    PubMed  Google Scholar 

  • Oroojloo M, Shariatpanahi ME (2011) Induction of multi-cellular structures in isolated microspores of roses (Rosa Hybrid). VII Int Symp Vitro Cult Hortic Breed 961:479–486

    Google Scholar 

  • Peixe A, Barroso J, Potes A, Pais M (2004) Induction of haploid morphogenic calluses from in vitro cultured anthers of Prunus armeniaca Cv.‘Harcot’. PTOC 77(1):35–41

    Google Scholar 

  • Ravi M, Chan SWL (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464(7288):615–618

    PubMed  Google Scholar 

  • Ravi M, Shibata F, Ramahi JS, Nagaki K, Chen C, Murata M, Chan SWL (2011) Meiosis-specific loading of the centromere-specific histone CENH3 in Arabidopsis thaliana. PloS Genet 7(6):e1002121

    PubMed  PubMed Central  Google Scholar 

  • Ren J, Wu P, Trampe B, Tian X, Lübberstedt T, Chen S (2017) Novel technologies in doubled haploid line development. Plant Biotechnol J 15(11):1361–1370

    PubMed  PubMed Central  Google Scholar 

  • Sanei M, Pickering R, Kumke K, Nasuda S, Houben A (2011) Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci U S A 108(33):E498–E505

    PubMed  PubMed Central  Google Scholar 

  • Sohal B, Amandeep M, Arora N, Gill M, Malhotra P (2019) Anther culture for haploid production in guava (Psidium guajava L). Agric Res J 56(2):198–205

    Google Scholar 

  • Tek AL, Kashihara K, Murata M, Nagaki K (2010) Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon. Chromosome Res 18(3):337–347

    PubMed  Google Scholar 

  • Van der Veken J, Eeckhaut T, Baert J, Ruttink T, Maudoux O, Werbrouck S, Van Huylenbroeck J (2019) Cichorium intybus L.× Cicerbita Alpina Walbr: doubled haploid chicory induction and CENH3 characterization. Euphytica 215(7):1–13

    Google Scholar 

  • Van Dun CMP, Lelivelt CLC, Movahedi S (2018) Non-transgenic haploid inducer lines in cucurbits. U S Patent Application 15/774,779.

  • Wang N, Dawe RK (2018) Centromere size and its relationship to haploid formation in plants. Mol Plant 11(3):398–406

    PubMed  Google Scholar 

  • Wang G, He Q, Liu F, Cheng Z, Talbert PB, Jin W (2011) Characterization of CENH3 proteins and centromere-associated DNA sequences in diploid and allotetraploid Brassica species. Chromosoma 120(4):353–365

    PubMed  Google Scholar 

  • Wang S, Jin W, Wang K (2019) Centromere histone H3-and phospholipase-mediated haploid induction in plants. Plant Methods 15(1):1–10

    Google Scholar 

  • Wang N, Gent JI, Dawe RK (2021) Haploid induction by a maize CENH3 null mutant. Sci Adv 7(4):eabe2299

    PubMed  PubMed Central  Google Scholar 

  • Watts A, Kumar V, Bhat SR (2016) Centromeric histone H3 protein: from basic study to plant breeding applications. J Plant Biochem Biotechnol 25(4):339–348

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Zhang YX, Lespinasse YJA (1988) Culture in vitro d’ovules non fécondés et d’embryons prélevés 8 jours après pollinisation chez le pommier cultivé (Malus× Domestica Borkh). Agronomie 8(10):837–842

    Google Scholar 

Download references

Acknowledgements

AR and SSH acknowledges the support by the National Research Foundation of Korea (NRF) (Grant Nos. 2020R1A6A1A03044512, 2020R1A2C1012586) and the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through High Value-added Food Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (321027-5).

Author information

Authors and Affiliations

Authors

Contributions

Anjali Rai and Kavita Dubey have a contribution to planning and drafting this manuscript. Sung Soo Han have contributed in final editing and supervision throughout the manuscript preparation. All the authors have read and approved the final manuscript.

Corresponding author

Correspondence to Sung Soo Han.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest in the publication.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rai, A., Dubey, K. & Han, S.S. CENH3 mediated haploid induction: application and future perspectives in crop plants. Hortic. Environ. Biotechnol. 64, 1055–1069 (2023). https://doi.org/10.1007/s13580-023-00567-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13580-023-00567-2

Keywords

Navigation