The Inheritable Characteristics of Monoecy and Parthenogenesis Provide A Means for Establishing A Doubled Haploid Population in the Economically Important Brown Alga Undariapinnatifida (Laminariales, Alariaceae)

Abstract

Monoecy and parthenogenesis exist in certain male and female gametophytes of the brown alga Undaria pinnatifida. The inheritance of these traits is not known. In this study, we made a cross between a male and a female gametophyte clone which could exhibit monoecy and parthenogenesis phenotypes, respectively, and obtained their next‐generation gametophyte offspring. We found that under conditions suitable for gametogenesis, all of the male offspring (n = 100) exhibited monoecy phenotype and all of the female offspring (n = 100) only formed oogonia and underwent parthenogenesis, suggesting that monoecy and parthenogenesis phenotypes are inheritable. Then, we established a doubled haploid (DH) population through monoecious selfing and parthenogenesis, and evaluated the young sporophyte growth and the maximum quantum yield (Fv/Fm) of 10 “male” and 10 “female” DH lines. On day 60, the average length of the “male” DH lines was significantly larger than that of the “female” DH lines, while their average Fv/Fm values were not significantly different. Monoecious selfing seemed superior to parthenogenesis as the sporophyte formation efficiency, and the young sporophyte growth was better in the former than in the latter. We also crossed two monoecious gametophytes with another male gametophyte, and a parentage analysis showed success of obtaining hybrid sporophytes, indicating that the female gametes released by the monoecious gametophyte can actually be fertilized by sperm. The approach of establishing a DH population proposed here will be useful in genetic breeding and quantitative trait loci mapping in U. pinnatifida and may be applicable to other kelp species.

Breeding in the Economically Important Brown Alga Undaria pinnatifida: A Concise Review and Future Prospects

“…They are determined to be haploid by flow cytometry analysis, different from the diploid gametophyte derived from tissue culture of the sporophyte thalli ( Zhang et al, 2007 ; Shan et al, 2020b ). Microsatellite analysis confirmed that hybrid sporophytes could be obtained when the monoicous gametophyte was crossed with another male gametophyte, which indicates the eggs discharged by the monoicous gametophyte can really be fertilized by sperm, and thus they have the same sexual function as those discharged by the female gametophytes ( Shan et al, 2021 ). They can also self-breed to give rise to doubled haploid (DH) sporophytes, albeit the fertilization rate of the eggs during selfing is much lower than during outcrossing.…”

“…It may be partly tackled by using the DH sporophytes resulting from monoicous selfing and parthenogenesis of certain paternal and maternal gametophyte lines ( Figure 1 ). Monoicy phenotype has been shown to be more common than expected in cultivated strains ( Li et al, 2014 ; Shan et al, 2021 ). The fecundity of mature DH sporophytes is high, being able to release millions of spores with the same genotype as that of the corresponding parental gametophyte ( Shan et al, 2013 ; Shan et al, 2021 ).…”

“…Monoicy phenotype has been shown to be more common than expected in cultivated strains ( Li et al, 2014 ; Shan et al, 2021 ). The fecundity of mature DH sporophytes is high, being able to release millions of spores with the same genotype as that of the corresponding parental gametophyte ( Shan et al, 2013 ; Shan et al, 2021 ). Hence, DH sporophytes can be utilized in crossbreeding to scale up the production by circumventing the laborious and time-consuming propagation of gametophyte filaments.…”

“…They can also self-breed to give rise to doubled haploid (DH) sporophytes, albeit the fertilization rate of the eggs during selfing is much lower than during outcrossing. Despite the low fertilization rate in selfing, most of the derived sporophytes are morphologically normal, suggesting they are generated through self-fertilization (sexual reproduction) rather than parthenogenesis which usually results in a high ratio of abnormal parthenosporophytes ( Shan et al, 2021 ).…”

“…The method is also applicable to other kelp species. According to a cross experiment, it has also been found that the monoicous and parthenogenetic phenotypes of the parental gametophytes of U. pinnatifida are able to be inherited to the next gametophyte generation after meiosis within the hybrid sporophyte ( Shan et al, 2021 ). Such an inheritable feature makes it possible to establish DH lines by exploiting phenotypes of monoicy and parthenogenesis.…”