Genomic selection in algae with biphasic lifecycles: A Saccharina latissima (sugar kelp) case study

Huang, Mao; Robbins, Kelly R.; Li, Yaoguang; Umanzor, Schery; Marty-Rivera, Michael; Bailey, David; Aydlett, Margaret; Schmutz, Jeremy; Grimwood, Jane; Yarish, Charles; Lindell, Scott; Jannink, Jean-Luc

doi:10.3389/fmars.2023.1040979

Title: Genomic selection in algae with biphasic lifecycles: A Saccharina latissima (sugar kelp) case study

Journal Article · 22 February 2023 · Frontiers in Marine Science

DOI: https://doi.org/10.3389/fmars.2023.1040979 · OSTI ID:1958253

Huang, Mao; Robbins, Kelly R.; Li, Yaoguang; Umanzor, Schery; Marty-Rivera, Michael; Bailey, David; Aydlett, Margaret; Schmutz, Jeremy; Grimwood, Jane; Yarish, Charles; Lindell, Scott; Jannink, Jean-Luc

Introduction Sugar kelp ( Saccharina latissima ) has a biphasic life cycle, allowing selection on both thediploid sporophytes (SPs) and haploid gametophytes (GPs). Methods We trained a genomic selection (GS) model from farm-tested SP phenotypic data and used a mixed-ploidy additive relationship matrix to predict GP breeding values. Topranked GPs were used to make crosses for further farm evaluation. The relationship matrix included 866 individuals: a) founder SPs sampled from the wild; b) progeny GPs from founders; c) Farm-tested SPs crossed from b); and d) progeny GPs from farm-tested SPs. The complete pedigree-based relationship matrix was estimated for all individuals. A subset of founder SPs ( n = 58) and GPs ( n = 276) were genotyped with Diversity Array Technology and whole genome sequencing, respectively. We evaluated GS prediction accuracy via cross validation for SPs tested on farm in 2019 and 2020 using a basic GBLUP model. We also estimated the general combining ability (GCA) and specific combining ability (SCA) variances of parental GPs. A total of 11 yield-related and morphology traits were evaluated. Results The cross validation accuracies for dry weight per meter ( r ranged from 0.16 to 0.35) and wet weight per meter ( r ranged 0.19 to 0.35) were comparable to GS accuracy for yield traits in terrestrial crops. For morphology traits, cross validation accuracy exceeded 0.18 in all scenarios except for blade thickness in the second year. Accuracy in a third validation year (2021) was 0.31 for dry weight per meter over a confirmation set of 87 individuals. Discussion Our findings indicate that progress can be made in sugar kelp breeding by using genomic selection.

View Journal Article

Cite

Export

Save

Research Organization:: Woods Hole Oceanographic Institution, Woods Hole, MA (United States)

Sponsoring Organization:: USDOE; USDOE Advanced Research Projects Agency - Energy (ARPA-E)

Grant/Contract Number:: AR0000915

OSTI ID:: 1958253

Journal Information:: Frontiers in Marine Science, Journal Name: Frontiers in Marine Science Vol. 10; ISSN 2296-7745

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

References (71)

Strong population structure but no equilibrium yet: Genetic connectivity and phylogeography in the kelpSaccharina latissima(Laminariales, Phaeophyta) Luttikhuizen, Pieternella C.; van den Heuvel, Freek H. M.; Rebours, Céline Ecology and Evolution, Vol. 8, Issue 8 https://doi.org/10.1002/ece3.3968	journal	April 2018
Genetics of Morphology and Growth in Laminaria from the North Atlantic Ocean — Implications for Biogeography Egan, B.; Garcia-Ezquivel, Z.; Brinkhuis, B. H. Evolutionary Biogeography of the Marine Algae of the North Atlantic https://doi.org/10.1007/978-3-642-75115-8_8	book	January 1990
Relationships among analytical methods used to study genotypic variation and genotype-by-environment interaction in plant breeding multi-environment experiments Cooper, M.; DeLacy, I. H. Theoretical and Applied Genetics, Vol. 88, Issue 5 https://doi.org/10.1007/BF01240919	journal	July 1994
Accuracy of genomic selection in European maize elite breeding populations Zhao, Yusheng; Gowda, Manje; Liu, Wenxin Theoretical and Applied Genetics, Vol. 124, Issue 4 https://doi.org/10.1007/s00122-011-1745-y	journal	November 2011
A reaction norm model for genomic selection using high-dimensional genomic and environmental data Jarquín, Diego; Crossa, José; Lacaze, Xavier Theoretical and Applied Genetics, Vol. 127, Issue 3 https://doi.org/10.1007/s00122-013-2243-1	journal	December 2013
Genomic selection across multiple breeding cycles in applied bread wheat breeding Michel, Sebastian; Ametz, Christian; Gungor, Huseyin Theoretical and Applied Genetics, Vol. 129, Issue 6 https://doi.org/10.1007/s00122-016-2694-2	journal	April 2016
Genomic selection for wheat traits and trait stability Huang, Mao; Cabrera, Antonio; Hoffstetter, Amber Theoretical and Applied Genetics, Vol. 129, Issue 9 https://doi.org/10.1007/s00122-016-2733-z	journal	June 2016
Efficiency of multi-trait, indirect, and trait-assisted genomic selection for improvement of biomass sorghum Fernandes, Samuel B.; Dias, Kaio O. G.; Ferreira, Daniel F. Theoretical and Applied Genetics, Vol. 131, Issue 3 https://doi.org/10.1007/s00122-017-3033-y	journal	December 2017
Commercial cultivation and bioremediation potential of sugar kelp, Saccharina latissima, in Danish waters Marinho, Gonçalo S.; Holdt, Susan L.; Birkeland, Mads J. Journal of Applied Phycology, Vol. 27, Issue 5 https://doi.org/10.1007/s10811-014-0519-8	journal	January 2015
Characterization of newly developed expressed sequence tag-derived microsatellite markers revealed low genetic diversity within and low connectivity between European Saccharina latissima populations Guzinski, Jaromir; Mauger, Stéphane; Cock, J. Mark Journal of Applied Phycology, Vol. 28, Issue 5 https://doi.org/10.1007/s10811-016-0806-7	journal	March 2016
Cultivation of a morphologically distinct strain of the sugar kelp, Saccharina latissima forma angustissima, from coastal Maine, USA, with implications for ecosystem services Augyte, Simona; Yarish, Charles; Redmond, Sarah Journal of Applied Phycology, Vol. 29, Issue 4 https://doi.org/10.1007/s10811-017-1102-x	journal	April 2017
Combined effects of seasonal variation and drying methods on the physicochemical properties and antioxidant activity of sugar kelp (Saccharina latissima) Sappati, Praveen Kumar; Nayak, Balunkeswar; VanWalsum, G. Peter Journal of Applied Phycology, Vol. 31, Issue 2 https://doi.org/10.1007/s10811-018-1596-x	journal	August 2018
Fermentation of sugar kelp (Saccharina latissima)—effects on sensory properties, and content of minerals and metals Bruhn, Annette; Brynning, Gunhild; Johansen, Aase Journal of Applied Phycology, Vol. 31, Issue 5 https://doi.org/10.1007/s10811-019-01827-4	journal	July 2019
Prospects for upgrading by the European kelp sector van den Burg, Sander; Selnes, Trond; Alves, Liliana Journal of Applied Phycology, Vol. 33, Issue 1 https://doi.org/10.1007/s10811-020-02320-z	journal	November 2020
The nitrogen bioextraction potential of nearshore Saccharina latissima cultivation and harvest in the Western Gulf of Maine Grebe, G. S.; Byron, C. J.; Brady, D. C. Journal of Applied Phycology, Vol. 33, Issue 3 https://doi.org/10.1007/s10811-021-02367-6	journal	February 2021
Skinny kelp (Saccharina angustissima) provides valuable genetics for the biomass improvement of farmed sugar kelp (Saccharina latissima) Li, Yaoguang; Umanzor, Schery; Ng, Crystal Journal of Applied Phycology, Vol. 34, Issue 5 https://doi.org/10.1007/s10811-022-02811-1	journal	August 2022
Use of genomic selection in breeding rice (Oryza sativa L.) for resistance to rice blast (Magnaporthe oryzae) Huang, Mao; Balimponya, Elias G.; Mgonja, Emmanuel M. Molecular Breeding, Vol. 39, Issue 8 https://doi.org/10.1007/s11032-019-1023-2	journal	July 2019
Genome-wide association analysis reveals new insights into the genetic architecture of defensive, agro-morphological and quality-related traits in cassava Rabbi, Ismail Yusuf; Kayondo, Siraj Ismail; Bauchet, Guillaume Plant Molecular Biology, Vol. 109, Issue 3 https://doi.org/10.1007/s11103-020-01038-3	journal	July 2020
Mariculture of the Asian kelp Undaria pinnatifida and the native kelp Saccharina latissima along the Atlantic coast of Southern Europe: An overview Peteiro, César; Sánchez, Noemí; Martínez, Brezo Algal Research, Vol. 15 https://doi.org/10.1016/j.algal.2016.01.012	journal	April 2016
Polar lipid profile of Saccharina latissima, a functional food from the sea Rey, Felisa; Lopes, Diana; Maciel, Elisabete Algal Research, Vol. 39 https://doi.org/10.1016/j.algal.2019.101473	journal	May 2019
Growth and agarose characteristics of isomorphic gametophyte (male and female) and sporophyte of Gracilaria dura and their marker assisted selection Gupta, Vishal; Baghel, Ravi S.; Kumar, Manoj Aquaculture, Vol. 318, Issue 3-4 https://doi.org/10.1016/j.aquaculture.2011.06.009	journal	August 2011
The cultivation of European kelp for bioenergy: Site and species selection Kerrison, Philip D.; Stanley, Michele S.; Edwards, Maeve D. Biomass and Bioenergy, Vol. 80 https://doi.org/10.1016/j.biombioe.2015.04.035	journal	September 2015
The use of unbalanced historical data for genomic selection in an international wheat breeding program Dawson, Julie C.; Endelman, Jeffrey B.; Heslot, Nicolas Field Crops Research, Vol. 154 https://doi.org/10.1016/j.fcr.2013.07.020	journal	December 2013
Improving gaseous biofuel yield from seaweed through a cascading circular bioenergy system integrating anaerobic digestion and pyrolysis Deng, Chen; Lin, Richen; Kang, Xihui Renewable and Sustainable Energy Reviews, Vol. 128 https://doi.org/10.1016/j.rser.2020.109895	journal	August 2020
Genomic imprinting: parental influence on the genome Reik, Wolf; Walter, Jörn Nature Reviews Genetics, Vol. 2, Issue 1 https://doi.org/10.1038/35047554	journal	January 2001
Cryptic genetic variation: evolution's hidden substrate Paaby, Annalise B.; Rockman, Matthew V. Nature Reviews Genetics, Vol. 15, Issue 4 https://doi.org/10.1038/nrg3688	journal	March 2014
Genomic prediction for hastening and improving efficiency of forward selection in conifer polycross mating designs: an example from white spruce Lenz, Patrick R. N.; Nadeau, Simon; Azaiez, Aïda Heredity, Vol. 124, Issue 4 https://doi.org/10.1038/s41437-019-0290-3	journal	January 2020
Opportunities, challenges and future directions of open-water seaweed aquaculture in the United States Kim, JangKyun; Stekoll, Michael; Yarish, Charles Phycologia, Vol. 58, Issue 5 https://doi.org/10.1080/00318884.2019.1625611	journal	September 2019
Genomic selection in plant breeding: from theory to practice Jannink, J. -L.; Lorenz, A. J.; Iwata, H. Briefings in Functional Genomics, Vol. 9, Issue 2 https://doi.org/10.1093/bfgp/elq001	journal	February 2010
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Fast and accurate long-read alignment with Burrows–Wheeler transform Li, Heng; Durbin, Richard Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btp698	journal	January 2010
Improving SNP discovery by base alignment quality Li, H. Bioinformatics, Vol. 27, Issue 8 https://doi.org/10.1093/bioinformatics/btr076	journal	February 2011
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
Simulation of sugar kelp (Saccharina latissima) breeding guided by practices to accelerate genetic gains Huang, Mao; Robbins, Kelly R.; Li, Yaoguang G3 Genes\|Genomes\|Genetics, Vol. 12, Issue 3 https://doi.org/10.1093/g3journal/jkac003	journal	January 2022
Prediction of Total Genetic Value Using Genome-Wide Dense Marker Maps Meuwissen, T. H. E.; Hayes, B. J.; Goddard, M. E. Genetics, Vol. 157, Issue 4 https://doi.org/10.1093/genetics/157.4.1819	journal	April 2001
Functional properties of the isomorphic biphasic algal life cycle Thornber, C. S. Integrative and Comparative Biology, Vol. 46, Issue 5 https://doi.org/10.1093/icb/icl018	journal	June 2006
Systematic Procedures for Calculating Inbreeding Coefficients Emik, L. Otis; Terrill, Clair E. Journal of Heredity, Vol. 40, Issue 2 https://doi.org/10.1093/oxfordjournals.jhered.a105986	journal	February 1949
Comparative analysis of morphometric traits of farmed sugar kelp and skinny kelp, Saccharina spp., strains from the Northwest Atlantic Umanzor, Schery; Li, Yaoguang; Bailey, David Journal of the World Aquaculture Society, Vol. 52, Issue 5 https://doi.org/10.1111/jwas.12783	journal	March 2021
The importance of information on relatives for the prediction of genomic breeding values and the implications for the makeup of reference data sets in livestock breeding schemes Clark, Samuel A.; Hickey, John M.; Daetwyler, Hans D. Genetics Selection Evolution, Vol. 44, Issue 1 https://doi.org/10.1186/1297-9686-44-4	journal	February 2012
A molecular timescale of eukaryote evolution and the rise of complex multicellular life Hedges, S.; Blair, Jaime E.; Venturi, Maria L. BMC Evolutionary Biology, Vol. 4, Issue 1, p. 2 https://doi.org/10.1186/1471-2148-4-2	journal	January 2004
Accuracy of genomic selection in simulated populations mimicking the extent of linkage disequilibrium in beef cattle Brito, Fernanda V.; Neto, José; Sargolzaei, Mehdi BMC Genetics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2156-12-80	journal	January 2011
Stability of Genomic Selection prediction models across ages and environments Resende, Marcio FR; Muñoz Del Valle, Patricio R.; Acosta, Juan J. BMC Proceedings, Vol. 5, Issue S7 https://doi.org/10.1186/1753-6561-5-S7-O14	journal	September 2011
Genetic Map Construction and Quantitative Trait Locus (QTL) Detection of Six Economic Traits Using an F2 Population of the Hybrid from Saccharina longissima and Saccharina japonica Zhang, Jing; Liu, Tao; Feng, Rongfang PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0128588	journal	May 2015
On the Accuracy of Genomic Selection Rabier, Charles-Elie; Barre, Philippe; Asp, Torben PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156086	journal	June 2016
Red seaweed (Asparagopsis taxiformis) supplementation reduces enteric methane by over 80 percent in beef steers Roque, Breanna M.; Venegas, Marielena; Kinley, Robert D. PLOS ONE, Vol. 16, Issue 3 https://doi.org/10.1371/journal.pone.0247820	journal	March 2021
European aquaculture of sugar kelp (Saccharina latissima) for food industries: iodine content and epiphytic animals as major problems Lüning, Klaus; Mortensen, Leiv Botanica Marina, Vol. 58, Issue 6 https://doi.org/10.1515/bot-2015-0036	journal	November 2015
Effectiveness of Genomic Prediction of Maize Hybrid Performance in Different Breeding Populations and Environments Windhausen, Vanessa S.; Atlin, Gary N.; Hickey, John M. G3 Genes\|Genomes\|Genetics, Vol. 2, Issue 11 https://doi.org/10.1534/g3.112.003699	journal	November 2012
Shrinkage Estimation of the Realized Relationship Matrix Endelman, Jeffrey B.; Jannink, Jean-Luc G3: Genes\|Genomes\|Genetics, Vol. 2, Issue 11 https://doi.org/10.1534/g3.112.004259	journal	November 2012
Genomic Selection for Yield and Seed Composition Traits Within an Applied Soybean Breeding Program Stewart-Brown, Benjamin B.; Song, Qijian; Vaughn, Justin N. G3 Genes\|Genomes\|Genetics, Vol. 9, Issue 7 https://doi.org/10.1534/g3.118.200917	journal	July 2019
Factors Affecting Accuracy From Genomic Selection in Populations Derived From Multiple Inbred Lines: A Barley Case Study Zhong, Shengqiang; Dekkers, Jack C. M.; Fernando, Rohan L. Genetics, Vol. 182, Issue 1 https://doi.org/10.1534/genetics.108.098277	journal	March 2009
Prediction of Genetic Values of Quantitative Traits in Plant Breeding Using Pedigree and Molecular Markers Crossa, José; Campos, Gustavo de los; Pérez, Paulino Genetics, Vol. 186, Issue 2 https://doi.org/10.1534/genetics.110.118521	journal	September 2010
Multiple-Trait Genomic Selection Methods Increase Genetic Value Prediction Accuracy Jia, Yi; Jannink, Jean-Luc Genetics, Vol. 192, Issue 4 https://doi.org/10.1534/genetics.112.144246	journal	October 2012
Genomic Selection in Plant Breeding: A Comparison of Models Heslot, Nicolas; Yang, Hsiao-Pei; Sorrells, Mark E. Crop Science, Vol. 52, Issue 1 https://doi.org/10.2135/cropsci2011.06.0297	journal	January 2012
Modeling Genotype × Environment Interaction for Genomic Selection with Unbalanced Data from a Wheat Breeding Program Lado, Bettina; Barrios, Pablo González; Quincke, Martín Crop Science, Vol. 56, Issue 5 https://doi.org/10.2135/cropsci2015.04.0207	journal	September 2016
Introduction to a Special Issue on Genotype by Environment Interaction de Leon, Natalia; Jannink, Jean-Luc; Edwards, Jode W. Crop Science, Vol. 56, Issue 5 https://doi.org/10.2135/cropsci2016.07.0002in	journal	September 2016
The Accuracy of Genomic Prediction between Environments and Populations for Soft Wheat Traits Huang, Mao; Ward, Brian; Griffey, Carl Crop Science, Vol. 58, Issue 6 https://doi.org/10.2135/cropsci2017.10.0638	journal	September 2018
Speciation in the exposed intertidal zone: the case of Saccharina angustissima comb. nov . & stat. nov . (Laminariales, Phaeophyceae) Augyte, Simona; Lewis, Louise; Lin, Senjie Phycologia, Vol. 57, Issue 1 https://doi.org/10.2216/17-40.1	journal	January 2018
Fine-scale population genetic structure of sugar kelp, Saccharina latissima (Laminariales, Phaeophyceae), in eastern Maine, USA Breton, Timothy S.; Nettleton, Jeremy C.; O'Connell, Brennah Phycologia, Vol. 57, Issue 1 https://doi.org/10.2216/17-72.1	journal	January 2018
Enhancing Hybrid Prediction in Pearl Millet Using Genomic and/or Multi-Environment Phenotypic Information of Inbreds Jarquin, Diego; Howard, Reka; Liang, Zhikai Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.01294	journal	January 2020
Population Genetics of Sugar Kelp Throughout the Northeastern United States Using Genome-Wide Markers Mao, Xiaowei; Augyte, Simona; Huang, Mao Frontiers in Marine Science, Vol. 7 https://doi.org/10.3389/fmars.2020.00694	journal	August 2020
Combining Partially Overlapping Multi-Omics Data in Databases Using Relationship Matrices Akdemir, Deniz; Knox, Ron; Isidro y. Sánchez, Julio Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00947	journal	July 2020
Scalable Sparse Testing Genomic Selection Strategy for Early Yield Testing Stage Atanda, Sikiru Adeniyi; Olsen, Michael; Crossa, Jose Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.658978	journal	June 2021
Key Considerations for the Use of Seaweed to Reduce Enteric Methane Emissions From Cattle Vijn, Sandra; Compart, Devan Paulus; Dutta, Nikki Frontiers in Veterinary Science, Vol. 7 https://doi.org/10.3389/fvets.2020.597430	journal	December 2020
Changes in the Composition of Atlantic Salmon upon the Brown Seaweed (Saccharina latissima) Treatment Kirkholt, Even Moen; Dikiy, Alexander; Shumilina, Elena Foods, Vol. 8, Issue 12 https://doi.org/10.3390/foods8120625	journal	November 2019
Seascape Genomics of the Sugar Kelp Saccharina latissima along the North Eastern Atlantic Latitudinal Gradient Guzinski, Jaromir; Ruggeri, Paolo; Ballenghien, Marion Genes, Vol. 11, Issue 12 https://doi.org/10.3390/genes11121503	journal	December 2020
Genome-Wide Mapping of Cytosine Methylation Revealed Dynamic DNA Methylation Patterns Associated with Sporophyte Development of Saccharina japonica Yang, Xiaoqi; Wang, Xiuliang; Yao, Jianting International Journal of Molecular Sciences, Vol. 22, Issue 18 https://doi.org/10.3390/ijms22189877	journal	September 2021
Accuracy and Training Population Design for Genomic Selection on Quantitative Traits in Elite North American Oats Asoro, Franco G.; Newell, Mark A.; Beavis, William D. The Plant Genome, Vol. 4, Issue 2 https://doi.org/10.3835/plantgenome2011.02.0007	journal	July 2011
Ridge Regression and Other Kernels for Genomic Selection with R Package rrBLUP Endelman, Jeffrey B. The Plant Genome Journal, Vol. 4, Issue 3 https://doi.org/10.3835/plantgenome2011.08.0024	journal	January 2011
Assessing Genomic Selection Prediction Accuracy in a Dynamic Barley Breeding Population Sallam, A. H.; Endelman, J. B.; Jannink, J. ‐L. The Plant Genome, Vol. 8, Issue 1 https://doi.org/10.3835/plantgenome2014.05.0020	journal	March 2015
Genetic Gain from Phenotypic and Genomic Selection for Quantitative Resistance to Stem Rust of Wheat Rutkoski, J.; Singh, R. P.; Huerta-Espino, J. The Plant Genome, Vol. 8, Issue 2 https://doi.org/10.3835/plantgenome2014.10.0074	journal	July 2015
Seaweed aquaculture: cultivation technologies, challenges and its ecosystem services Kim, Jang K.; Yarish, Charles; Hwang, Eun Kyoung ALGAE, Vol. 32, Issue 1 https://doi.org/10.4490/algae.2017.32.3.3	journal	March 2017

Similar Records

Skinny kelp (Saccharina angustissima) provides valuable genetics for the biomass improvement of farmed sugar kelp (Saccharina latissima)

Journal Article · 2022 · Journal of Applied Phycology · OSTI ID:1882750

Li, Yaoguang; Umanzor, Schery; Ng, Crystal; +7 more

Evaluation of genomic selection and marker-assisted selection in Miscanthus and energycane

Journal Article · 2019 · Molecular Breeding · OSTI ID:1618382

Olatoye, Marcus O.; Clark, Lindsay V.; Wang, Jianping; +4 more

Biomass yield improvement in switchgrass through genomic prediction of flowering time

Journal Article · 2022 · Global Change Biology. Bioenergy · OSTI ID:1876364

Tilhou, Neal W.; Casler, Michael D.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biphasic cycle
breeding
brown algae
genomic selection (GS)
genotyping
phenotyping
sugar kelp (Saccharina latissima)

Title: Genomic selection in algae with biphasic lifecycles: A Saccharina latissima (sugar kelp) case study

Citation Formats

References (71)

Similar Records

Related Subjects