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Cytological Analysis of Male-Sterile MS5 Japanese Cedar (Cryptomeria japonica D. Don) and Comparison with Other Male-Sterile Mutants

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Abstract

Cryptomeria japonica D. Don is a model plant for studying male sterility in conifers. To date, five male sterile loci have been identified by crossing tests. When at least one of these loci is homozygote of a recessive male sterile allele, male sterility is induced. Cytological studies have been performed for ms1 to ms4 mutants, but there have yet to be such investigations of ms5 mutants. This study newly showed that ms2 mutants lack callose and exhibit different phenotypes for each microsporangium. Furthermore, we found the leakage of cellular contents and the appearance of amorphous substances in ms3 mutants. We also detected leakage of cellular contents in ms4 mutants. On the other hand, abnormal pollen development in ms5 mutants was found to begin at the tetrad stage. This abnormality was characterized by the maintenance of abnormal tetrads and uneven spores, abnormal pollen wall formation, covered with amorphous substances, disappearance of the nucleus, and central nuclear positioning during the binuclear microspore stage. These results were clearly different from those of ms1 to ms4 mutants. Abnormal meiosis in pollen mother cells, the abnormal pollen wall, and abnormal mitosis during pollen development may be closely associated with male sterility caused by mutation of MS5.

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The datasets used and/or analyzed in this study are available from the corresponding author up-on reasonable request.

References

  • Andersson E (1947) A case of asyndesis in Picea abies. Hereditas 33:301–347

    Article  Google Scholar 

  • Bhojwani SS, Bhatnagar SP, Dantu PK (2015) Microsporangium (chapter 3) and male gametophyte-development (chapter 4). The embryology of angiosperms, 6th edn. Vikas Publishing House, New Delhi, pp 14–57

    Google Scholar 

  • Bione NCP, Pagliarini MS, Almedia LA (2002) An original mutation in soybean (Glycine max (L.) Merrill) involving degeneration of the generative cell and causing male sterility. Genome 45:1257–1261

    Article  PubMed  Google Scholar 

  • Borkakati RP, Virmani SS (1996) Genetics of thermosensitive genic male sterility in rice. Euphytica 88:1–7

    Article  Google Scholar 

  • Chen YCS, McCormick S (1996) Sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development 122:3243–3253

    Article  CAS  PubMed  Google Scholar 

  • Chen SH, Chung NJ, Wang YN, Lee CL, Lee YL, Tsai PF (2006) Study of male sterility in Taiwania cryptomerioides Hayata (Taxodiaceae). Protoplasma 228:137–144

    Article  PubMed  Google Scholar 

  • Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19:847–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forest Tree Gene Symbol Notation Committee (2016) Revised standardization of genetic symbols for forest trees. For Genet Tree Breed 5:134–137 (in Japanese)

    Google Scholar 

  • Fujino T, Yamaguchi K, Yokoyama TT, Hamanaka T, Harazono Y, Kamada H, Kobayashi W, Ujino-Ihara T, Uchiyama K, Matsumoto A, Izuno A, Tsumura Y, Toyoda A, Shigenobu S, Moriguchi Y, Ueno S, Kasahara M (2023) A chromosome-level genome assembly of a model conifer plant, the Japanese cedar, Cryptomeria japonica D. Don. bioRxiv

  • Futamura N, Kogawara S, Saito M, Higuchi Y, Watanabe K, Shinohara K (2013) Morphological characteristics of pollen grains in Shindai1 and Shindai5, male-sterile trees of Cryptomeria japonica during microgenesis. Kanto J for Res 64:61–64 (in Japanese with English abstract)

    Google Scholar 

  • Futamura N, Igasaki T, Saito M, Taira H, Shinohara K (2019) Comparison of fertile and sterile male gametogenesis in Cryptomeria japonica D. Don. Tree Genet Genomes 15:30

    Article  Google Scholar 

  • Grienenberger E, Kim SS, Lallemand B, Geoffroy P, Heintz D, de Azevedo SC, Heitz T, Douglas CJ, Legrand M (2010) Analysis of TETRAKETIDE α-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Plant Cell 22:4067–4083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa Y, Ueno S, Wei FJ, Matsumoto A, Uchiyama K, Ujino-Ihara T, Hakamata T, Fujino T, Kasahara M, Bino T, Yamaguchi K, Shigenobu S, Tsumura Y, Moriguchi Y (2021) Identification and genetic diversity analysis of a male-sterile gene (MS1) in Japanese cedar (Cryptomeria japonica D. Don). Sci Rep 11:1496

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Hirayama S, Iwai J, Higuchi Y, Kaneko T, Moriguchi Y (2021) Selection of trees with male sterile genes except for MALE STERILITY 1 in Cryptomeria japonica D. Don. J Jpn For Soc 103:161–167 (in Japanese with English abstract)

    Article  Google Scholar 

  • Hosoo Y, Yoshii E, Negishi K, Taira H (2005) A histological comparison of the development of pollen and female gametophytes in fertile and sterile Cryptomeria japonica. Sex Plant Reprod 18:81–89

    Article  Google Scholar 

  • Igarashi M, Watanabe J, Ozawa H, Saito Y, Taira H (2004) The male sterile sugi (Cryptomeria japonica D. Don) was found in Fukushima Prefecture (I): selection of the search ground and identification of the male sterility. Tohoku J For Sci 9:86–89 (in Japanese with English abstract)

    Google Scholar 

  • Igarashi M, Watanabe J, Saito H, Ozawa S, Saito N, Furukawa S, Ishii Y (2006) Breeding for low pollen sugi (Cryptomeria japonica D. Don.). Fukushima Pref For Res Cent Res 39:1–9 (in Japanese)

    Google Scholar 

  • Kakui H, Ujino-Ihara T, Hasegawa Y, Tsurisaki E, Futamura N, Iwai J, Higuchi Y, Fujino T, Suzuki Y, Kasahara M, Yamaguchi K, Shigenobu S, Otani M, Nakao M, Ueno S, Moriguchi Y (2023) A single-nucleotide substitution of CjTKPR1 determines pollen production in the gymnosperm plant Cryptomeria japonica. PNAS Nexus 2:1–8

    Article  Google Scholar 

  • Kaul MLH (1988) Male sterility in higher plants. Springer, Berlin

    Book  Google Scholar 

  • Kawana M, Yoshii E, Taira H (2006) Mechanism of female sterility in sugi (Cryptomeria japonica D. Don). J Jpn For Soc 88:156–159 (in Japanese with English abstract)

    Article  Google Scholar 

  • Khoshoo TN (1957) Cytology of conifers III. Partial failure of meiotic spindle in Cephalotaxus drupacea var. pedunculata. Cytologia 22:80–89

    Article  Google Scholar 

  • Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot Rev 38:425–454

    Article  Google Scholar 

  • Maâtaoui ME, Pichot C (2001) Microsporogenesis in the endangered species Cupressus dupreziana A. Camus: evidence for meiotic defects yielding unreduced and abortive pollen. Planta 213:543–549

    Article  PubMed  Google Scholar 

  • Miura S, Nameta M, Yamamoto T, Igarashi M, Taira H (2011) Mechanisms of male sterility in four Cryptomeria japonica individuals with obvious visible abnormality at the tetrad stage. J Jpn For Soc 93:1–7 (in Japanese with English abstract)

    Article  Google Scholar 

  • Miyajima D, Yoshii E, Hosoo Y, Taira H (2010) Cytological and genetic studies on male sterility in Cryptomeria japonica D. Don (Shindai 8). J Jpn For Soc 92:106–109 (in Japanese with English abstract)

    Article  Google Scholar 

  • Moriguchi Y, Ujino-Ihara T, Uchiyama K, Futamura N, Saito M, Ueno S, Matsumoto A, Tani N, Taira H, Shinohara K, Tsumura Y (2012) The construction of a high-density linkage map for identifying SNP markers that are tightly linked to a nuclear-recessive major gene for male sterility in Cryptomeria japonica D. Don. BMC Genomics 13:95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moriguchi Y, Ueno S, Higuchi Y, Miyajima D, Itoo S, Futamura N, Shinohara K, Tsumura Y (2014) Establishment of a microsatellite panel covering the sugi (Cryptomeria japonica) genome, and its application for localization of a male-sterile gene (ms-2). Mol Breed 33:315–325

    Article  CAS  Google Scholar 

  • Moriguchi Y, Uchiyama K, Ueno S, Ujino-Ihara T, Matsumoto A, Iwai J, Miyajima D, Saito M, Sato M, Tsumura Y (2016) A high-density linkage map with 2,560 markers and its application for the localization of the male-sterile genes ms3 and ms4 in Cryptomeria japonica D. Don. Tree Genet Genomes 12:57

    Article  Google Scholar 

  • Moriguchi Y, Ueno S, Hasegawa Y, Tadama T, Watanabe M, Saito R, Hirayama S, Iwai J, Konno Y (2020) Marker-assisted selection of trees with MALE STERILITY 1 in Cryptomeria japonica D. Don. Forests 11:734

    Article  Google Scholar 

  • Orr-Ewing AL (1978) Partial male sterility in Douglas fir. Province of British Columbia Ministry of Forests Research Memo 35

  • Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen 1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799

    Article  CAS  PubMed  Google Scholar 

  • Pichot C, Maâtaoui ME (2000) Unreduced diploid nuclei in Cupressus dupreziana A. Camus pollen. Theor Appl Genet 101:574–579

    Article  Google Scholar 

  • Runquist EW (1968) Meiotic investigations in Pinus silvestris (L). Hereditas 60:77–128

    Article  Google Scholar 

  • Saito M (2010) Breeding strategy for the pollinosis preventive cultivars of Cryptomeria japonica D. Don J Jpn For Soc 92:316–323 (in Japanese with English abstract)

    Article  Google Scholar 

  • Saito H (2017) Sterility found in both staminate and pistillate flowers of Japanese Cypress (Chamaecyparis obtusa (Sieb. et Zucc.) Endl.). J Jpn For Soc 99:150–155 (in Japanese with English abstract)

    Article  ADS  Google Scholar 

  • Saito H (2020) Development and verification of precision of a simple screening method for male sterility in seedling production of apanese cedar (Cryptomeria japonica D. Don). J Jpn For Soc 102:311–316 (in Japanese with English abstract)

    Article  Google Scholar 

  • Saito M, Taira H, Furuta Y (1998) Cytological and genetical studies on male sterility in Cryptomeria japonica D. Don. J For Res 3:167–173

    Article  Google Scholar 

  • Schneider CA, Rasband WA, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taira H, Teranishi H, Kenda Y (1993) A case study of male sterility in sugi (Cryptomeria japonica). J Jpn For Soc 75:377–379 (in Japanese with English abstract)

    Google Scholar 

  • Taira H, Saito M, Furuta Y (1999) Inheritance of the trait of male sterility in Cryptomeria japonica. J For Res 4:271–273

    Article  Google Scholar 

  • Takahashi M, Iwaizumi MG, Hoshi H, Kubota M, Fukuda Y, Fukatsu E, Kondo T (2007) Survey of male sterility on sugi (Cryptomeria japonica D. Don) clones collected from Kanto Breeding Region and characteristics of two male-sterile clones. Bull Natl For Tree Breed Cent 23:11–36 (in Japanese with English abstract)

    Google Scholar 

  • Tsubomura M, Kurita M, Watanabe A (2016) Determination of male strobilus developmental stages by cytological and gene expression analyses in Japanese cedar (Cryptomeria japonica). Tree Physiol 36:653–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchiya T, Toriyama K, Yoshikawa M, Ejiri S, Hinata K (1995) Tapetum-specific expression of the gene for an endo-β-1,3-glucanase causes male sterility in transgenic tobacco. Plant Cell Physiol 36:487–494

    Article  CAS  PubMed  Google Scholar 

  • Twell D, Park SK, Lalanne E (1998) Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci 3:305–310

    Article  Google Scholar 

  • Ueuma H, Yoshii E, Hosoo Y, Taira H (2009) Cytological study of a male-sterile Cryptomeria japonica that does not release microspores from tetrads. J For Res 14:123–126

    Article  Google Scholar 

  • Van der Kley FK (1954) Male sterility and its importance in breeding heterosis varieties. Euphytica 3:117–124

    Article  Google Scholar 

  • Vedel F, Pla M, Vitart V, Gutierres S, Chetrit P, Paepe RD (1994) Molecular basis of nuclear and cytoplasmic male sterility in higher plants. Plant Physiol Biochem 32:601–608

    CAS  Google Scholar 

  • Wang Y, Lin YC, So J, Du Y, Lo C (2013) Conserved metabolic steps for sporopollenin precursor formation in tobacco and rice. Physiol Plant 149:13–24

    Article  CAS  PubMed  ADS  Google Scholar 

  • Watanabe M, Ueno S, Hasegawa Y, Moriguchi Y (2022) Efficient low-cost marker-assisted selection of trees with MALE STERILITY 1 (MS1) in Japanese cedar (Cryptomeria japonica D. Don) using bulk DNA samples. Tree Genet Genomes 18:29

    Article  CAS  Google Scholar 

  • Wilson VR, Owens JN (2003) Histology of sterile male and female cones in Pinus monticola (western white pine). Sex Plant Reprod 15:301–310

    Article  Google Scholar 

  • Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in Transgenic Tobacco. Plant Cell 4:759–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, Qu S, Tucker MR, Zhang D, Liang W, Shi J (2019) Ostkpr1 functions in anther cuticle development and pollen wall formation in rice. BMC Plant Biol 19:104

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada H, Yamaguchi K (2009) Survey of male sterility of sugi (Cryptomeria japonica D. Don) clones collected from Kansai Breeding Region and characteristics of the male-sterile clone. Appl For Sci 8:33–36 (in Japanese)

    Google Scholar 

  • Yoshii E, Taira H (2007) Cytological and genetical studies on male sterile sugi (Cryptomeria japonica D. Don), Shindai 1 and Shindai 5. J Jpn For Soc 89:26–30 (in Japanese with English abstract)

    Article  Google Scholar 

  • Zhou H, Zhou M, Yang Y, Li J, Zhu L, Jiang D, Dong J, Liu Q, Gu L, Zhou L, Feng M, Qin P, Hu X, Song C, Shi J, Song X, Ni E, Wu X, Deng Q, Liu Z, Chen M, Liu YG, Cao X, Zhuang C (2014) RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5:4884

    Article  CAS  PubMed  ADS  Google Scholar 

  • Zhu L, Zhang T, Teeri TH (2021) Tetraketide α-pyrone reductases in sporopollenin synthesis pathway in Gerbera hybrida: diversification of the minor function. Hort Res 8:207

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Junko Kumagai, Kenji Ohyachi and Yasuko Hayashi for technical support of microscope and TEM observation, respectively.

Funding

This research was supported by JSPS KAKENHI (21K05666) and Niigata University U-go grant to YM.

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Authors and Affiliations

  1. Department of Environmental Science and Technology, Graduate School of Science and Technology, Niigata University, Niigata, Japan

    Eriko Tsurisaki

  2. Division of Microscopic Anatomy, Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan

    Masaaki Nameta & Shinsuke Shibata

  3. Niigata Prefectural Government, Niigata Regional Promotion Bureau, Niigata, Japan

    Satoko Hirayama

  4. Niigata Prefectural Forest Research Institute, Niigata, Japan

    Junji Iwai & Yukiko Ito

  5. Division of Molecular and Diagnostic Pathology, Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan

    Riuko Ohashi

  6. Department of Agriculture, Faculty of Agriculture, Niigata University, Niigata, Japan

    Masahiro Otani, Nana Matsumura & Yoshinari Moriguchi

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  1. Eriko Tsurisaki
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  2. Masaaki Nameta
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  10. Yoshinari Moriguchi
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Contributions

YM, SS, MN, MO and RO conceived and designed research. SH, JI and YI prepared materials. ET, MN and NM performed experiments. ET and YM wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Yoshinari Moriguchi.

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Tsurisaki, E., Nameta, M., Shibata, S. et al. Cytological Analysis of Male-Sterile MS5 Japanese Cedar (Cryptomeria japonica D. Don) and Comparison with Other Male-Sterile Mutants. J. Plant Biol. 67, 11–23 (2024). https://doi.org/10.1007/s12374-023-09415-3

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