Abstract
It has become increasingly important to understand the factors controlling the abundance of male strobili in Cryptomeria japonica since allergic reactions to the species’ pollen have become prevalent in Japan. There is considerable inter-annual variation in the abundance of male strobili, so it is important to investigate and validate quantitative trait loci (QTL) for strobili abundance across different years. Data on third generation families derived from an individual that produces abundant male strobili were studied using Kruskal–Wallis tests and Bayesian regression analysis, resulting in the detection of a single major QTL that was observed over multiple years. This QTL explained between 10.4 and 26.5 % of the phenotypic variation in male strobilus abundance. The consistency and significance of this QTL’s effects suggest that it has a major role in male strobilus production in C. japonica, although we also detected other QTLs, indicating that strobilus production is subject to complex and multifactorial regulation. These QTL may also affect precocity because we were unable to separate their effects from the genetic variability in male strobilus production. The major QTL that we detected occurs in a region homologous to a QTL detected in a previous study examining trees with a different genetic heritage following artificial induction of male strobilus production. This result further supports the importance of the QTL detected in the present study. Identifying the important genes in this QTL will therefore significantly increase our understanding of the genetic mechanisms of pollen production in C. japonica.
Similar content being viewed by others
References
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890
Catterou M, Dubois F, Smets R, Vaniet S, Kichey T, Van Onckelen H, Sangwan-Norreel BS, Sangwan RS (2002) hoc: an Arabidopsis mutant overproducing cytokinins and expressing high in vitro organogenic capacity. Plant J 30:273–287
Cecich RA, Kang H, Chalupka W (1994) Regulation of early flowering in Pinus banksiana. Tree Physiol 14:275–284
Cheverud JM (2001) A simple correction for multiple comparisons in interval mapping genome scans. Heredity 87:52–58
Chiba F (1999) Studies on alleviating Sugi-pollinosis to a lower level in fields based on forestry technology. Bull of the Ibaraki Prefectural Gov For Technol Cent 25:1–32, in Japanese
Coolbaugh RC (1984) Inhibition of Ent-kaurene oxidation by cytokinins. J Plant Growth Regul 3:97–109
Costantini E, Landi L, Silvestroni O, Pandolfini T, Spena A, Mezzetti B (2007) Auxin synthesis-encoding transgene enhances grape fecundity. Plant Physiol 143:1689–1694
Fletcher JC (2001) The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 128:1323–1333
Fukui M, Futamura N, Mukai Y, Wang Y, Nagao A, Sinohara K (2001) Ancestral MADS box genes in sugi, Cryptomeria japonica D. Don (Taxodiaceae), homologous to the B function genes in angiosperm. Plant Cell Physiol 42:566–575
Futamura N, Totoki Y, Toyoda A, Igasaki T, Nanjo T, Seki M, Sakaki Y, Mari A, Shinozaki K, Shinohara K (2008) Characterization of expressed sequence tags from a full-length enriched cDNA library of Cryptomeria japonica male strobili. BMC Genom 9:383
Huang S, Cerny RE, Qi Y, Bhat D, Aydt CM, Hanson DD, Malloy KP, Ness LA (2003) Transgenic studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol 131:1270–1282
Imbault N, Doumas P, Joseph C, Bonnet-Masimbert M (1989) Changes in endogenous cytokinins during flowering induction in Douglas fir: effect of exogenous applications. Ann For Sci 46:40s–43s
Iwata H, Ebana K, Ebana K, Uga Y, Hayashi T, Jannink JL (2009) Genome-wide association study of grain shape variation among Oryza sativa L. germplasms based on elliptic Fourier analysis. Mol Breed 25:203–215
Khodakovskaya M, Zhao D, Smith W, Li Y, McAvoy R (2006) Expression of ipt gene controlled by an ethylene and auxin responsive fragment of the LEACO1 promoter increases flower number in transgenic Nicotiana tabacum. Plant Cell Rep 25:1181–1192
Kondo T (1994) Characteristics of male flower setting of elite tree of Cryptomeria japonica. Breed For Trees 172:19–22, in Japanese
Kosambi DD (1944) The estimation of map distances from recombination values. Annals Eugenics 12:172–175
Kurita M, Taniguchi T, Nakada R, Kondo T, Watanabe A (2011) Spatiotemporal gene expression profiles associated with male strobilus development in Cryptomeria japonica by suppression subtractive hybridization. Breed Sci 61:174–182
Liew M, Pryor R, Palais R, Meadows C, Erali M, Lyon E, Wittwer C (2004) Genotyping of single-nucleotide polymorphisms by high resolution melting of small amplicons. Clin Chem 50:1156–1164
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 Genom 13:95
Nagao A, Sasaki S, Pharis RP (1989) Cryptomeria japonica. In: Halevy AH (ed) CRC handbook of flowering. CRC, Boca Raton, pp 247–269
Nickerson DA, Tobe VO, Taylor SL (1997) PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res 25:2745–2751
Okuda M (2003) Epidemiology of Japanese cedar pollinosis throughout Japan. Annals Allergy, Asthma Immunol 91:288–296
Pharis RP, Webber JE, Ross SD (1987) The promotion of flowering in forest trees by gibberellin A4/7 and cultural treatments: a review of the possible mechanisms. For Ecol Manag 19:65–84
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
Saito T, Kawasaki H (1984) Studies on flowering characteristics and their heredity in Cryptomeria japonica D. Don. Bull For For Prod Res Ins 328:17–41, in Japanese
Schmidtling RC (1981) The inheritance of precocity and its relationship with growth in loblolly pines. Silvae Genetica 30:188–192
Tani N, Takahashi T, Iwata H, Mukai Y, Ujino-Ihara T, Matsumoto A, Yoshimura K, Yoshimaru H, Murai M, Nagasaka K, Tsumura Y (2003) A consensus linkage map for sugi (Cryptomeria japonica) from two pedigrees, based on microsatellites and expressed sequence tags. Genetics 165:1551–1568
Ujino-Ihara T, Taguchi Y, Yoshimura K, Tsumura Y (2003) Analysis of expressed sequence tags derived from developing seed and pollen cones of Cryptomeria japonica. Plant Biol 5:600–607
Van Ooijen JW, Voorrips RE (2001) JoinMap version 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0, software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen
Yi N, George V, Allison DB (2003) Stochastic search variable selection for identifying multiple quantitative trait loci. Genetics 164:1129–1138
Yoshimaru H, Ohba K, Tsurumi K, Tomaru N, Murai M, Mukai Y, Suyama Y, Tsumura Y, Kawahara T, Sakamaki Y (1998) Detection of quantitative trait loci for juvenile growth, flower bearing and rooting ability based on a linkage map of sugi (Cryptomeria japonica). Theor Appl Genet 97:45–50
Acknowledgments
This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (grant no. 15780118) and by the Program for Supporting Activities for Female Researchers funded by the Special Coordination Fund for Promoting Science and Technology of the Ministry of Education, Culture, Sports, Science and Technology, Japan, and the Program for the Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry. The authors would like to thank Dr. H. Fukuoka for providing the protocol for the HRM analysis. The authors are also grateful to Ms. M. Koshiba for technical assistance and Messrs. M. Okamoto, K. Arai, I. Karube, H. Kimura, T. Suzuki, T. Yoshitake, and all members of the Tree Genetics laboratory at FFPRI for helping with field experiments and progeny maintenance. We also acknowledge Mr. M. Murai for supplying the pedigree of CR46.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by D. Grattapaglia
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PPTX 1101 kb)
ESM 2
Linkage maps for C. japonica. The linkage groups on the left are based on the consensus map from Tani et al. (2003) and the other linkage groups were constructed based on the segregation data of three third generation progenies derived from CR46. The prefixes A, B, and C were given before the number of each of the linkage groups for families A, B and C, respectively. In the consensus map, markers that are orthologous to those used in this study are indicated in bold and part of them are also indicated by allelic bridges. Markers that could not be positioned in the linkage groups constructed in this study are shown in italics. For HRM markers, corresponding cDNA clone names (or the name of corresponding markers on the consensus map) are shown after the HRM marker name (PPTX 1.07 MB)
ESM 3
(DOCX 129 kb)
Rights and permissions
About this article
Cite this article
Ujino-Ihara, T., Iwata, H., Taguchi, Y. et al. Identification of QTLs associated with male strobilus abundance in Cryptomeria japonica . Tree Genetics & Genomes 8, 1319–1329 (2012). https://doi.org/10.1007/s11295-012-0518-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-012-0518-3