Abstract
The inheritance of chloroplast genome DNA (cpDNA) differs from that of the nuclear genome. The cpDNAs of most species originate from the female parent, whereas some plastids are paternal or biparental in origin. The plastid transmission of Pinaceae species is thought to occur exclusively by paternal inheritance with a few exceptions. However, plastid transmission in a common species of Pinus (Pinaceae), Pinus massoniana, remains unexplored. In this study, 16 parents and 84 progenies from 9 full-sib families including one reciprocal cross were used as research materials, and a minisatellite locus and 3 cpDNA DNA fragments were used to investigate the plastid transmission of P. massoniana. The results showed that 96.73% of the offspring had cpDNA sequences consistent with those of their male parents, whereas only 3.27% of the offspring had cpDNA sequences similar to those of their female parents. These results revealed that plastid transmission in P. massoniana is predominantly paternal, mainly manifesting as high-frequency (greater than 95%) paternal inheritance and low-frequency maternal inheritance. However, the mechanism of paternal inheritance requires more evidence and further research.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All sequences have been submitted to GenBank (accession numbers: MT107910—MT108136).
References
Abdullah MF, Shahzadi I, Waseem S, Mirza B, Ahmed I, Waheed M (2020) Chloroplast genome of Hibiscus rosa-sinensis (Malvaceae): comparative analyses and identification of mutational hotspots. Genomics 112:581–591. https://doi.org/10.1016/j.ygeno.2019.04.010
Aravanopoulos FA, Drouzas AD, Wang XR, Panetsos KP & D Moulalis (2000) Preliminary results on the inheritance of the chloroplast genome in Pinus brutia Ten. In: Gozukirmizi, N., (ed) Proc. 2nd Balkan Botanical Congress, Istanbul, Turkey, 2: 195–200. https://doi.org/10.13140/RG.2.1.2021.7041.
Barnard-Kubow KB, McCoy MA, Galloway LF (2017) Biparental chloroplast inheritance leads to rescue from cytonuclear incompatibility. New Phytologist 213:1466–1476. https://doi.org/10.1111/nph.14222
Bruns D, Owens JN (2000) Western white pine (Pinus monticola Dougl.) reproduction: II. Fertilisation and cytoplasmic inheritance. Sex Plant Reprod 13:75–84. https://doi.org/10.1007/s004970000041
Cafasso D, Cozzolino S, Caputo P, De Luca P (2001) Maternal inheritance of plastids in Encephalartos Lehm. (Zamiaceae, Cycadales). Genome 44:239–241. https://doi.org/10.1139/gen-44-2-239
Chen J, Tauer C, Huang Y (2002) Paternal chloroplast inheritance patterns in pine hybrids detected with trnL–trnF intergenic region polymorphism. Theor App Genet 104:1307–1311. https://doi.org/10.1007/s00122-002-0893-5
Cipriani G, Testolin R, Morgante M (1995) Paternal inheritance of plastids in interspecific hybrids of the genus Actinidia revealed by PCR-amplification of chloroplast DNA fragments. Mol Gen Genet 247:693–697. https://doi.org/10.1007/bf00290400
Crosby K, Smith DR (2012) Does the mode of plastid inheritance influence plastid genome architecture? PLoS ONE 7(9):e46260. https://doi.org/10.1371/journal.pone.0046260
Dong J, Wagner DB, Yanchuk AD, Carlson MR, Magnussen S, Wang X-R, Szmidt AE (1992) Paternal chloroplast DNA inheritance in Pinus contora and Pinus banksiana: independence of parenetal species or cross direction. J Here 83:419–422. https://doi.org/10.1093/oxfordjournals.jhered.a111244
Fang X, Zhang F, Wu N, Hu S (2003) Plastid inheritance in sweet potato as revealed by DNA restriction fingerprinting. Acta Botanica Sinica 45:73–75. https://doi.org/10.3321/j.issn:1672-9072.2003.01.010
Gichira AW, Li Z, Saina JK, Long Z, Hu G, Gituru RW, Wang Q, Chen J (2017) The complete chloroplast genome sequence of an endemic monotypic genus Hagenia (Rosaceae): structural comparative analysis, gene content and microsatellite detection. PeerJ 5:e2846. https://doi.org/10.7717/peerj.2846
Greiner S, Sobanski J, Bock R (2015) Why are most organelle genomes transmitted maternally? BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology 37:80–94. https://doi.org/10.1002/bies.201400110
Guo F, Hu S-Y, Yuan Z, Zee S-Y, Han Y (2005) Paternal cytoplasmic transmission in Chinese pine (Pinus tabulaeformis). Protoplasma 225:5–14. https://doi.org/10.1007/s00709-005-0088-4
Hagemann R (1992) Plastid Genetics in Higher Plants. In: Herrmann RG (ed) Cell Organelles. Springer Vienna, Vienna, pp 65–96
Hagemann R, Schröder M-B (1989) The cytological basis of the plastid inheritance in angiosperms. Protoplasma 152:57–64. https://doi.org/10.1007/bf01323062
Hansen AK, Escobar LK, Gilbert LE, Jansen RK (2007) Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. Am J Bot 94:42–46. https://doi.org/10.3732/ajb.94.1.42
Katoh K, Standley DM (2013) Mafft multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kaundun SS, Matsumoto S (2011) Molecular evidence for maternal inheritance of the chloroplast genome in tea, Camellia sinensis (L.) O. Kuntze. J Sci Food Agric 91:2660–2663. https://doi.org/10.1002/jsfa.4508
Kondo T, Tsumura Y, Kawahara T, Okamura M (1998) Paternal inheritance of chloroplast and mitochondrial DNA in interspecific hybrids of Chamaecyparis spp. Breed Sci 48:177–179. https://doi.org/10.1270/jsbbs1951.48.177
Kong WQ, Yang JH (2017) The complete chloroplast genome sequence of Morus cathayana and Morus multicaulis, and comparative analysis within genus Morus L. PeerJ 5:e3037. https://doi.org/10.7717/peerj.3037
Kormutak A, Galgoci M, Manka P, Koubova M, Jopcik M, Sukenikova D, Bolecek P, Gomory D (2017) Field-based artificial crossings indicate partial compatibility of reciprocal crosses between Pinus sylvestris and Pinus mugo and unexpected chloroplast DNA inheritance. Tree Genetics & Genomes 13(3):1–13. https://doi.org/10.1007/s11295-017-1152-x
Kumari M, Clarke HJ, des Francs-Small CC, Small I, Khan TN, and Siddique KHM, (2011) Albinism does not correlate with biparental inheritance of plastid DNA in interspecific hybrids in Cicer species. Plant Science 180:628–633. https://doi.org/10.1016/j.plantsci.2011.01.003
Lee DJ, Blake TK, Smith SE (1988) Biparental inheritance of chloroplast DNA and the existence of heteroplasmic cells in alfalfa. Theoretical and Applied Genetics 76:545–549. https://doi.org/10.1007/bf00260905
Li D, Qi X, Li X, Li L, Zhong C, Huang H (2013) Maternal inheritance of mitochondrial genomes and complex inheritance of chloroplast genomes in Actinidia Lind.: evidences from interspecific crosses. Molecular Genetics and Genomics 288:101–110. https://doi.org/10.1007/s00438-012-0732-6
Marshall KA, Neale DB (1992) The inheritance of mitochondrial DNA in Douglas-fir (Pseudotsuga menziesii). Can J For Res 22(1):73–75. https://doi.org/10.1139/x92-010
Matsushima R, Hu Y, Toyoda K, Sodmergen Sakamoto W (2008) The model plant Medicago truncatula exhibits biparental plastid inheritance. Plant & Cell Physiology 49:81–89. https://doi.org/10.1093/pcp/pcm170
McKinnon GE, Vaillancourt RE, Tilyard PA, Potts BM (2001) Maternal inheritance of the chloroplast genome in Eucalyptus globulus and interspecific hybrids. Genome 44:831–835. https://doi.org/10.1139/g01-078
Mogensen HL (1996) The Hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404
Nagata N (2010) Mechanisms for independent cytoplasmic inheritance of mitochondria and plastids in angiosperms. J Plant Res 123(2):193–199. https://doi.org/10.1007/s10265-009-0293-x
Neale DB, Marshall KA, Sederoff RR (1989) Chloroplast and mitochondrial DNA are paternally inherited in Sequoia sempervirens D. Don Endl. Proceedings of the National Academy of Sciences of the United States of America 86(23):9347–9349. https://doi.org/10.1073/pnas.86.23.9347
Neale DB, Marshall KA, Harry DE (1991) Inheritance of chloroplast and mitochondrial DNA in incense-cedar (Calocedrus decurrens). Can J For Res 21(5):717–720. https://doi.org/10.1139/x91-100
Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor App Gen 77:212–216. https://doi.org/10.1007/bf00266189
Ni Z, Ye Y, Bai T, Xu M, Xu L (2017) Complete chloroplast genome of Pinus massoniana (Pinaceae): gene rearrangements, loss of ndh genes, and short inverted repeats contraction, expansion. Molecules 22:1528. https://doi.org/10.3390/molecules22091528
Ohba K (1971) Paternal transmission of a plastid anomaly in some reciprocal crosses of Sugi, Cryptomeria japonica. Silvae Genetica 20:101–107
Qi W, Yang H, Xue Y, Hu S (1999) Inheritance of chloroplast and mitochondrial DNA in Chinese fir (Cunninghamia lanceolata). Acta Botanica Sinica 41:695–699
Runions CJ, Owens JN (1999a) Sexual reproduction of interior Spruce (Pinaceae). I. Pollen germination to archegonial maturation. Int J Plant Sci 160:631–640. https://doi.org/10.1086/314170
Runions CJ, Owens JN (1999b) Sexual reproduction of interior Spruce (Pinaceae). II. Fertilization to early embryo formation. Int J Plant Sci 160:641–652. https://doi.org/10.1086/314171
Schumann CM, Hancock JF (1989) Paternal inheritance of plastids in Medicago sativa. Theor App Gen 78:863–866. https://doi.org/10.1007/bf00266672
Smith S (1989) Biparental inheritance of organelles and its implications in crop improvement. Plant Breed Rev 6:361–393
Stine M, Sears BB, Keathley DE (1989) Inheritance of plastids in interspecific hybrids of blue spruce and white spruce. Theor App Gen 78:768–774. https://doi.org/10.1007/BF00266656
Stine M, Keathley DE (1990) Paternal inheritance of plastids in Engelmann Spruce x Blue Spruce Hybrids. J Hered 81(6):443–446. https://doi.org/10.1159/000153963
Sullivan A, Schiffthaler B, Thompson S, Street N, Wang X-R (2017) Interspecific plastome recombination reflects ancient reticulate evolution in Picea (Pinaceae). Mol Biol Evol 34 https://doi.org/10.1093/molbev/msx111
Szmidt AE, Aldén T, Hällgren J-E (1987) Paternal inheritance of chloroplast DNA in Larix. Plant Molecular Biology 9:59–64. https://doi.org/10.1007/bf00017987
Szmidt AE, El-Kassaby YA, Sigurgeirsson A, Aldèn T, Lindgren D, Hällgren J-E (1988) Classifying seedlots of Picea sitchensis and P. glauca in zones of introgression using restriction analysis of chloroplast DNA. Theor App Gen 76:841–845. https://doi.org/10.1007/bf00273669
Vaughn KC, Debonte LR, Wilson KG, Schaffer GW (1980) Organelle alteration as a mechanism for maternal inheritance. Science 208:196–198. https://doi.org/10.1126/science.208.4440.196
Vrancken J, Wesselingh RA (2010) Inheritance of the chloroplast genome in Rhinanthus angustifolius (Orobanchaceae). Plant Ecol Evol 143:239–242. https://doi.org/10.5091/plecevo.2010.425
Wagner DB, Furnier GR, Saghai-Maroof MA, Williams SM, Dancik BP, Allard RW (1987) Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proceedings of the National Academy of Sciences of the United States of America 84:2097–2100. https://doi.org/10.1073/pnas.84.7.2097
Weihe A, Apitz J, Pohlheim F, Salinas-Hartwig A, Börner T (2009) Biparental inheritance of plastidial and mitochondrial DNA and hybrid variegation in Pelargonium. Mol Geneti Genom 282:587–593. https://doi.org/10.1007/s00438-009-0488-9
Wilson K, Vaughn K (1979) Organelle destruction, a new mechanism to explain maternal inheritance of plastids and mitochondria in higher-plants. Plant Physiology: Amer Soc Plant Physiologists 15501 Monona Drive Rockville, Md 20855 5 5
ZhangSodmergen Q (2010) Why does biparental plastid inheritance revive in angiosperms? J Plant Res 123:201–206. https://doi.org/10.1007/s10265-009-0291-z
Zheng W, Chen J, Hao Z, Shi J (2016) Comparative analysis of the chloroplast genomic information of Cunninghamia lanceolata (Lamb.) Hook with sibling species from the genera Cryptomeria D. Don, Taiwania Hayata, and Calocedrus Kurz. Int J Mol Sci 17:1084. https://doi.org/10.3390/ijms17071084
Acknowledgements
We would like to thank Yabin Chen, Wenjiang Lin, and Yifa Huang for their help in sample collection. The authors are also grateful to the anonymous reviewers and editors for their constructive comments.
Funding
This work was supported by the Natural Science Foundation of Jiangsu Province (No. BK20200772), Guangxi Science and Technology Plan Project “Research and development of high generation breeding technology and germplasm innovation of Pinus massoniana” (Gui Ke AD16380010) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Author information
Authors and Affiliations
Contributions
X.L. and N.Z. conceived and designed the experiments. N.Z., Z.P., Y.X., and M.X. collected samples and managed the materials. N.Z., Z.P., and X.Y. performed the experiments. N.Z. and M.X. analyzed the data. N.Z. wrote the paper. X.L. and M.X. revised the manuscript. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by J. Beaulieu
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
About this article
Cite this article
Ni, Z., Zhou, P., Xin, Y. et al. Parent–offspring variation transmission in full-sib families revealed predominantly paternal inheritance of chloroplast DNA in Pinus massoniana (Pinaceae). Tree Genetics & Genomes 17, 36 (2021). https://doi.org/10.1007/s11295-021-01519-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-021-01519-6