Sexual dimorphism in the dioecious willow Salix purpurea.
Melampsora
Salicaceae
ZW sex determination
bioenergy
dioecy
nitrogen utilization
rust
sexual dimorphism
willow
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
30
03
2020
accepted:
28
01
2021
pubmed:
19
8
2021
medline:
23
9
2021
entrez:
18
8
2021
Statut:
ppublish
Résumé
The evolution of sex chromosomes is driven by sexual dimorphism, yet it can be challenging to document sexually dimorphic traits in dioecious plant species. At the genetic level, sexual dimorphism can be identified through sequence variation between females and males associated with sexually antagonistic traits and different fitness optima. This study aims to examine sexual dimorphism for 26 traits in three populations of Salix purpurea (a diversity panel and F Sexual dimorphism was evaluated for morphological, phenological, physiological, and wood composition traits in a diversity panel of unrelated S. purpurea accessions and in full-sib F We observed sexual dimorphism in the timing of development for several traits that were highly predictive of biomass yield across three populations of S. purpurea. Across all populations and years surveyed, males had significantly shallower branching angle. Male plants highly predictive of biomass yield across three populations of S. purpurea also accumulated more nitrogen under fertilizer amendment as measured by SPAD in the diversity panel and had greater susceptibility to the rust fungus Melampsora americana in the F These results provide evidence of sexual dimorphism for certain traits in S. purpurea that may be involved in sex chromosome evolution.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1374-1387Informations de copyright
© 2021 Botanical Society of America.
Références
Arevalo, C. B. M., T. A. Volk, E. Bevilacqua, and L. Abrahamson. 2007. Development and validation of aboveground biomass estimations for four Salix clones in central New York. Biomass and Bioenergy 31: 1-12.
Arnold, S. J. 1994. Bateman's principles and the measurement of sexual selection in plants and animals. American Naturalist 144: S126-S149.
Bañuelos, M.-J., M. Sierra, and J.-R. Obeso. 2004. Sex, secondary compounds and asymmetry. Effects on plant-herbivore interaction in a dioecious shrub. Acta Oecologica 25: 151-157.
Bates, D., M. Mächler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1-48.
Boecklen, W. J., S. Mopper, and P. W. Price. 1994. Sex-biased herbivory in arroyo willow: Are there general patterns among herbivores? Oikos 71: 267-272.
Boecklen, W. J., P. W. Price, and S. Mopper. 1990. Sex and drugs and herbivores: sex-biased herbivory in arroyo willow (Salix lasiolepis). Ecology 71: 581-588.
Brown, H. P. 1921. Trees of New York state: Native and naturalized, vol. XXI, no. 5. Syracuse University, Syracuse, New York, USA.
Carlson, C. H., F. E. Gouker, L. B. Smart, C. R. Crowell, C. D. Smart, L. Evans, and S. P. DiFazio. 2019. Joint linkage and association mapping of complex traits in shrub willow (Salix purpurea L.). Annals of Botany 124: 701-715.
Carolyn, S. W., and P. W. Rundel. 1979. Sexual dimorphism and resource allocation in male and female shrubs of Simmondsia chinensis. Oecologia 44: 34-39.
Ceulemans, R., A. J. S. McDonald, and J. S. Pereira. 1996. A comparison among eucalypt, poplar and willow characteristics with particular reference to a coppice, growth-modelling approach. Biomass and Bioenergy 11: 215-231.
Charlesworth, D. 1999. Theories of the evolution of dioecy. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 33-60. Springer, Berlin, Germany.
Charlesworth, D. 2015. Plant contributions to our understanding of sex chromosome evolution. New Phytologist 208: 52-65.
Chave, J., D. Coomes, S. Jansen, S. L. Lewis, N. G. Swenson, and A. E. Zanne. 2009. Towards a worldwide wood economics spectrum. Ecological Letters 12: 351-366.
Chen, Y., T. Wang, L. Fang, X. Li, and T. Yin. 2016. Confirmation of single-locus sex determination and female heterogamety in willow based on linkage analysis. PLoS One 11: e0147671.
Collinson, M. E. 1992. The early fossil history of Salicaceae: A brief review. Proceedings of the Royal Society of Edinburgh, B, Biological Sciences 98B: 155-167.
Dawson, T. E., and M. A. Geber. 1999. Sexual dimorphism in physiology and morphology. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 175-215. Springer, Berlin Germany.
Delph, L. F. 1999. Sexual dimorphism in life history. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 149-173. Springer, Berlin, Germany.
Dickmann, D., and J. Kuzovkina 2008. Poplars and willows in the world, with emphasis on silviculturally important species. In J. G. Isebrands and J. Richardson [eds.], Poplars and willows: Trees for society and the environment, 8-91. Food and Agriculture Organization, Rome, Italy; CABI, Wallingford, UK.
Dudley, L. S., and C. Galen. 2007. Stage-dependent patterns of drought tolerance and gas exchange vary between sexes in the alpine willow, Salix glauca. Oecologia 153: 1-9.
Ehlers, B. K., and T. Bataillon. 2007. ‘Inconstant males’ and the maintenance of labile sex expression in subdioecious plants. New Phytologist 174: 194-211.
Feng, G., B. J. Sanderson, K. Keefover-Ring, J. Liu, T. Ma, T. Yin, L. B. Smart, et al. 2020. Pathways to sex determination in plants: How many roads lead to Rome? Current Opinion in Plant Biology 54: 61-68.
Gouker, F. E., S. P. DiFazio, B. Bubner, M. Zander, and L. B. Smart. 2019. Genetic diversity and population structure of native, naturalized, and cultivated Salix purpurea. Tree Genetics & Genomes 15: 47.
Hanley, S. J., M. H. Pei, S. J. Powers, C. Ruiz, M. D. Mallott, J. H. A. Barker, and A. Karp. 2011. Genetic mapping of rust resistance loci in biomass willow. Tree Genetics & Genomes 7: 597-608.
Hou, J., N. Ye, D. Zhang, Y. Chen, L. Fang, X. Dai, and T. Yin. 2015. Different autosomes evolved into sex chromosomes in the sister genera of Salix and Populus. Scientific Reports 5: 1-6.
Hultine, K. R., K. C. Grady, T. E. Wood, S. M. Shuster, J. C. Stella, and T. G. Whitham. 2016. Climate change perils for dioecious plant species. Nature Plants 2: 16109.
Kuzovkina, Y. A., and M. F. Quigley. 2005. Willows beyond wetlands: uses of Salix L. species for environmental projects. Water, Air, and Soil Pollution 162: 183-204.
Lewis, D. 1942. The evolution of sex in flowering plants. Biological Reviews 17: 46-67.
Lin, J., J. P. Gibbs, and L. B. Smart. 2009. Population genetic structure of native versus naturalized sympatric shrub willows (Salix: Salicaceae). American Journal of Botany 96: 771-785.
Lloyd, D. G., and C. J. Webb. 1977. Secondary sex characters in plants. Botanical Review 43: 177-216.
McCracken, A. R., and W. M. Dawson. 2003. Rust disease (Melampsora epitea) of willow (Salix spp.) grown as short rotation coppice (SRC) in inter- and intra-species mixtures. Annals of Applied Biology 143: 381-393.
Moritz, K. K., C. Björkman, A. L. Parachnowitsch, and J. A. Stenberg. 2016. Female Salix viminalis are more severely infected by Melampsora spp. but neither sex experiences associational effects. Ecology and Evolution 6: 1154-1162.
Obeso, J. R. 2002. The costs of reproduction in plants. New Phytologist 155: 321-348.
Pei, M. H., K. Lindegaard, C. Ruiz, and C. Bayon. 2008. Rust resistance of some varieties and recently bred genotypes of biomass willows. Biomass & Bioenergy 32: 453-459.
Pucholt, P., A.-C. Rönnberg-Wästljung, and S. Berlin. 2015. Single locus sex determination and female heterogamety in the basket willow (Salix viminalis L.). Heredity 114: 575-583.
R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website: https://www.R-project.org/
Renner, S. S. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany 101: 1588-1596.
Rönnberg-Wästljung, A.-C., B. Samils, V. Tsarouhas, and U. Gullberg. 2008. Resistance to Melampsora larici-epitea leaf rust in Salix: analyses of quantitative trait loci. Journal of Applied Genetics 49: 321-331.
Samils, B., A.-C. Rönnberg-Wästljung, and J. Stenlid. 2011. QTL mapping of resistance to leaf rust in Salix. Tree Genetics & Genomes 7: 1219-1235.
Sanderson, B. J., G. Feng, N. Hu, C. H. Carlson, L. B. Smart, K. Keefover-Ring, T. Yin, et al. 2021. Sex determination through X-Y heterogamety in Salix nigra. Heredity 126: 630-639.
Sanderson, B. J., L. Wang, P. Tiffin, Z. Wu, and M. S. Olson. 2019. Sex-biased gene expression in flowers, but not leaves, reveals secondary sexual dimorphism in Populus balsamifera. New Phytologist 221: 527-539.
Seger, J., and V. M. Eckhart. 1996. Evolution of sexual systems and sex allocation in plants when growth and reproduction overlap. Proceedings of the Royal Society, B, Biological Sciences 263: 833-841.
Semerikov, V., U. Lagercrantz, V. Tsarouhas, A. Rönnberg-Wästljung, C. Alström-Rapaport, and M. Lascoux. 2003. Genetic mapping of sex-linked markers in Salix viminalis L. Heredity 91: 293-299.
Serapiglia, M. J., F. E. Gouker, and L. B. Smart. 2014. Early selection of novel triploid hybrids of shrub willow with improved biomass yield relative to diploids. BMC Plant Biology 14: 74.
Smart, L. B., and K. D. Cameron. 2008. Genetic improvement of willow (Salix spp.) as a dedicated bioenergy crop. In W. Vermerris [ed.], Genetic improvement of bioenergy crops, 377-396. Springer, NY, NY, USA.
Stott, K. G. 1992. Willows in the service of man. Proceedings of the Royal Society of Edinburgh, B, Biological Sciences 98: 169-182.
Sun, G., Q. Ji, D. L. Dilcher, S. Zheng, K. C. Nixon, and X. Wang. 2002. Archaefructaceae, a new basal angiosperm family. Science 296: 899-904.
Tharakan, P. J., T. A. Volk, C. A. Nowak, and G. J. Ofezu. 2008. Assessment of canopy structure, light interception, and light-use efficiency of first year regrowth of shrub willow (Salix sp.). Bioenergy Research 1: 229-238.
Tuskan, G. A., S. DiFazio, S. Jansson, J. Bohlmann, I. Grigoriev, U. Hellsten, N. Putnam, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
Ueno, N., Y. Suyama, and K. Seiwa. 2007. What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis? Journal of Ecology 95: 951-959.
Vega-Frutis, R., M. A. Munguía-Rosas, S. Varga, and M.-M. Kytöviita. 2013. Sex-specific patterns of antagonistic and mutualistic biotic interactions in dioecious and gynodioecious plants. Perspectives in Plant Ecology, Evolution and Systematics 15: 45-55.
Weih, M. 2009. Genetic and environmental variation in spring and autumn phenology of biomass willows (Salix spp.): effects on shoot growth and nitrogen economy. Tree Physiology 29: 1479-1490.
Westergaard, M. 1958. The mechanism of sex determination in dioecious flowering plants. Advances in Genetics 9: 217-281.
Zhou, R., D. Macaya-Sanz, E. Rodgers-Melnick, C. H. Carlson, F. E. Gouker, L. M. Evans, J. Schmutz, et al. 2018. Characterization of a large sex determination region in Salix purpurea L. (Salicaceae). Molecular Genetics and Genomics 293: 1437-1452.