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Genomic Diversity of 39 Samples of Pyropia Species Grown in Japan

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Genomic Diversity of 39 Samples of Pyropia Species Grown in Japan bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.099044; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Genomic diversity of 39 samples of Pyropia species 2 grown in Japan 3 4 5 Yukio Nagano1¶*, Kei Kimura2¶, Genta Kobayashi2, and Yoshio Kawamura2 6 1Analytical Research Center for Experimental Sciences, Saga University, 1 Honjo-machi, Saga, 7 Japan 8 2Faculty of Agriculture, Saga University, 1 Honjo-machi, Saga, Japan 9 10 * Corresponding author 11 E-mail: [email protected] (YN) 12 13 ¶These authors contributed equally to this work. 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.099044; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 14 Abstract 15 Some Pyropia species, such as nori (P. yezoensis), are important marine crops. We conducted a 16 phylogenetic analysis of 39 samples of Pyropia species grown in Japan using organellar genome 17 sequences. A comparison of the chloroplast DNA sequences with those from China showed a clear 18 genetic separation between Japanese and Chinese P. yezoensis. Conversely, comparing the 19 mitochondrial DNA sequences did not separate Japanese and Chinese P. yezoensis. Analysis of 20 organellar genomes showed that the genetic diversity of Japanese P. yezoensis used in this study is 21 lower than that of Chinese wild P. yezoensis. To analyze the genetic relationships between samples 22 of Japanese Pyropia, we used whole-genome resequencing to analyze their nuclear genomes. In the 23 offspring resulting from cross-breeding between P. yezoensis and P. tenera, nearly 90% of the 24 genotypes analyzed by mapping were explained by the presence of different chromosomes 25 originating from two different parental species. Although the genetic diversity of Japanese P. 26 yezoensis is low, analysis of nuclear genomes genetically separated each sample. Samples isolated 27 from the sea were often genetically similar to those being farmed. Study of genetic heterogeneity of 28 samples within a single aquaculture strain of P. yezoensis showed that samples were divided into two 29 groups and the samples with frequent abnormal budding formed a single, genetically similar group. 30 The results of this study will be useful for breeding and the conservation of Pyropia species. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.099044; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 31 Introduction 32 The genus Pyropia is a marine red alga belonging to the family Bangiaceae. Within the genus 33 Pyropia, P. yezoensis Ueda (Susabi-nori in Japanese) and P. haitanensis Chang et Zheng (tan-zicai in 34 Chinese) are economically important marine crops that are consumed in many countries [1]. These 35 are farmed in Japan, China and Korea. In recent years, they have been eaten as ingredients of sushi 36 and snacks around the world, and their consumption is increasing. Its production in 2018 was 2 37 million tonnes [2]. Other species are cultivated or wild, and some are occasionally used as edibles. 38 For example, P. t e ne ra Kjellman (Asakusa-nori in Japanese) was once cultivated in Japan but has 39 now been replaced by P. yezoensis in many places. P. yezoensis has also been shown to have 40 pharmacological and nutritional properties [reviewed in 3,4]. For example, a peptide derived from 41 this seaweed induces apoptosis in cancer cells [5,6]. The eicosapentaenoic acid-rich lipid has also 42 been shown to be beneficial to health by alleviating hepatic steatosis [7]. 43 Inter- and intraspecific genetic diversity of Pyropia has not been well studied genomically. 44 Studying the genomic diversity of Pyropia species is necessary for planning the breeding and 45 conservation of these seaweeds. This information is also important for the use of species that have 46 not been utilized previously. Especially, utilization of underutilized species and breeding are 47 important to address climate change. Prior to the genomic era, various studies analyzed the genetic 48 diversity of Pyropia species. For example, studies used the methods based on simple sequence repeat 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.099044; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 [8,9], DNA sequencing of several genes [10-28], amplified fragment length polymorphism [29,30], 50 and polymerase chain reaction-restriction fragment length polymorphism [31]. These previous 51 studies analyzed small regions of the genome. In addition, many of these previous studies analyzed 52 the genetic differences between species by phylogenetic analysis. In other words, few have analyzed 53 population structure or admixture within species. 54 However, few genomic approaches were applied to study the genetic diversity of Pyropia species. 55 For example, to study the genetic diversity of P. yezoensis in China, high-throughput DNA 56 sequencing analyzed variations in the organellar genome [32]. This study divided wild P. yezoensis 57 from Shandong Province, China, into three clusters. Several methods, such as restriction-site 58 associated DNA sequencing [33], genotyping by sequencing [34], and whole-genome resequencing 59 [35,36] use high-throughput DNA sequencing and can be applied to the analysis of the nuclear 60 genome. Among them, whole-genome resequencing is the most effective way to get a 61 comprehensive view of the entire nuclear genome. In general, whole-genome resequencing requires 62 short reads generated by high-throughput DNA sequencing. The short reads obtained from 63 whole-genome resequencing can be appropriate in another application, the de novo assembly of the 64 organellar genome [37]. Hence, short reads are useful for research on both the nuclear and organellar 65 genomes. Besides, whole-genome sequencing of the nuclear genome is suitable for analyzing the 66 population structure and admixture within a species. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.099044; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 67 The Ariake sound is located in the south-west of Japan (Fig 1). It has an area of 1,700 km2. It is 68 characterized by a tidal range of up to 6 m. This tidal range is effectively used for the cultivation of 69 seaweed. As a result, the Ariake sound is the most productive place for seaweed in Japan. 70 71 Fig 1. Positions of the isolation sites. The base map was produced using SimpleMappr 72 (https://www.simplemappr.net/). The Ariake sound is shown in red. 73 74 In this study, we conducted a phylogenetic analysis of 39 samples of Pyropia species grown in 75 Japan using chloroplast DNA sequences assembled from short reads. To analyze the population 76 structure and admixture, we also used whole-genome resequencing to analyze the nuclear genomes 77 of 34 samples of P. yezoensis, one sample of the closely related P. t e n e ra, and one sample of the 78 offspring resulting from cross-breeding between P. yezoensis and P. t en e r a. Particularly, we focused 79 on the analysis of some kinds of seaweed in the Ariake sound, Japan, where seaweed production is 80 active. 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.15.099044; this version posted May 6, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 81 Materials and Methods 82 83 Materials 84 The collection sites were represented on a map generated with SimpleMappr [38] (Fig 1) and 85 shown in Table 1. When the collection was performed, a single blade (a mixture of four types of 86 haploid cell) was isolated. Next, carpospores (diploid spores) were collected from this blade and 87 cultured. The culture of carpospores derived from single blade was defined as ‘culture’ in this study. 88 Sometimes, one of the cultures was selected for aquaculture, which was defined as ‘strain’ in this 89 study. A culture was also created from a strain, which is indicated in Table 1. Each culture was used 90 as a sample in this study. In Japan, various cultures/strains are preserved in various institutions. 91 Therefore, the acquisition of culture was not necessarily performed by the authors, so some cultures 92 were provided by other researchers. From these cultures, this study focused on those grown in the 93 Ariake sound. 6 bioRxiv preprint was notcertifiedbypeerreview)istheauthor/funder,whohasgrantedbioRxivalicensetodisplaypreprintinperpetuity.Itmade 94 Table 1. List of Pyropia samples doi: https://doi.org/10.1101/2020.05.15.099044 Sample Purification Species Collection site Isolat Notes name to became ion homozygous year Pyr_1 + P.
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