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Transcriptomic Profiling Provides Insights into Inbreeding Depression in Yesso Scallop Patinopecten yessoensis

  • Liang Zhao
  • Yangping Li
  • Jiarun Lou
  • Zhihui Yang
  • Huan Liao
  • Qiang Fu
  • Zhenyi Guo
  • Shanshan LianEmail author
  • Xiaoli Hu
  • Zhemin Bao
Original Article

Abstract

Inbreeding often causes a decline in biological fitness, known as inbreeding depression. In genetics study, inbreeding coefficient f gives the proportion by which the heterozygosity of an individual is reduced by inbreeding. With the development of high-throughput sequencing, researchers were able to perform deep approaches to investigate which genes are affected by inbreeding and reveal some molecular underpinnings of inbreeding depression. As one commercially important species, Yesso scallop Patinopecten yessoensis confront the same dilemma of inbreeding depression. To examine how inbreeding affects gene expression, we compared the transcriptome of two experimentally selfing families with inbreeding coefficient f reached 0.5 as well as one natural population (f ≈ 0) of P. yessoensis. A total of 24 RNA-Seq libraries were constructed using scallop adductor muscle, and eventually 676.56 M (96.85%) HQ reads were acquired. Based on differential gene analysis, we were able to identify nine common differentially expressed genes (DEGs) across the top-ranked 30 DEGs in both selfing families in comparation with the natural population. Remarkable, through weighted gene co-expression network analysis (WGCNA), five common DEGs were found enriched in the most significant inbreeding related functional module M14 (FDR = 1.64E-156), including SREBP1, G3BP2, SBK1, KIAA1161, and AATs-Glupro. These five genes showed significantly higher expression in self-bred progeny. Suggested by the genetic functional analysis, up-regulated SREBP1, G3BP2, and KIAA1161 may suggest a perturbing lipid metabolism, a severe inframammary reaction or immune response, and a stress-responsive behavior. Besides, the significant higher SBK1 and AATs-Glupro may reflect the abnormal cellular physiological situation. Together, these genetic aberrant transcriptomic performances may contribute to inbreeding depression in P. yessoensis, deteriorating the stress tolerance and survival phenotype in self-bred progeny. Our results would lay a foundation for further comprehensive understanding of bivalve inbreeding depression, which may potentially benefit the genetic breeding for scallop aquaculture.

Keywords

Inbreeding depression Bivalves Transcriptome Differential expression analysis WGCNA 

Notes

Author Contributions

SL, XH, and ZB conceived and designed the experiments; QF and LZ performed the experiments; YL analyzed the data; JL, ZY, HL, and ZG contributed reagents/materials/analysis tools; SL and LZ wrote the paper.

Funding

This work was supported by the National Natural Science Foundation of China [grant no. (31802295)], and Youth Talent Program Supported by Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao) [grant no. (2018-MFS-T06)].

Compliance with Ethical Standards

Data Availability

The transcriptomic data used in the present research can be achieved on SRA database (PRJNA515834).

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10126_2019_9907_MOESM1_ESM.xlsx (472 kb)
ESM 1 (XLSX 471 kb)

References

  1. Aleng NA, Sung YY, MacRae TH, Abd Wahid ME (2015) Non-lethal heat shock of the Asian green mussel, Perna viridis, promotes Hsp70 synthesis, induces thermotolerance and protects against Vibrio infection. PLoS One 10:e0135603CrossRefGoogle Scholar
  2. Anders S, Pyl PT, Huber W (2015) HTSeq--a python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169Google Scholar
  3. Beissbarth T, Speed TP (2004) GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics 20:1464–1465CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300Google Scholar
  5. Burnell G, Allan G (eds) (2009) New technologies in aquaculture: improving production efficiency, quality and environmental management. Oxford, Woodhead PublishingGoogle Scholar
  6. Caplins SA, Turbeville JM (2015) High rates of self-fertilization in a marine ribbon worm (Nemertea). Biol Bull 229:255–264CrossRefGoogle Scholar
  7. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796CrossRefGoogle Scholar
  8. de Boer RA, Eens M, Fransen E, Muller W (2015) Hatching asynchrony aggravates inbreeding depression in a songbird (Serinus canaria): an inbreeding-environment interaction. Evolution 69:1063–1068CrossRefGoogle Scholar
  9. Dheilly NM, Lelong C, Huvet A, Favrel P (2011) Development of a Pacific oyster (Crassostrea gigas) 31,918-feature microarray: identification of reference genes and tissue-enriched expression patterns. BMC Genomics 12:468CrossRefGoogle Scholar
  10. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 29:15–21CrossRefGoogle Scholar
  11. Enders LS, Nunney L (2012) Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster. Proc R Soc B Biol Sci 279:3756–3764CrossRefGoogle Scholar
  12. Fearnside JF, Dumas ME, Rothwell AR, Wilder SP, Cloarec O, Toye A, Blancher C, Holmes E, Tatoud R, Barton RH, Scott J, Nicholson JK, Gauguier D (2008) Phylometabonomic patterns of adaptation to high fat diet feeding in inbred mice. PLoS One 3:e1668CrossRefGoogle Scholar
  13. Fellous A, Labed-Veydert T, Locrel M, Voisin AS, Earley RL, Silvestre F (2018) DNA methylation in adults and during development of the self-fertilizing mangrove rivulus, Kryptolebias marmoratus. Ecol Evol 8:6016–6033CrossRefGoogle Scholar
  14. Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258CrossRefGoogle Scholar
  15. Frankham R, Ralls K (1998) Conservation biology - inbreeding leads to extinction. Nature 392:441–442CrossRefGoogle Scholar
  16. Fu X, Sun Y, Wang J, Xing Q, Zou J, Li R, Wang Z, Wang S, Hu X, Zhang L, Bao Z (2014) Sequencing-based gene network analysis provides a core set of gene resource for understanding thermal adaptation in Zhikong scallop Chlamys farreri. Mol Ecol Resour 14:184–198CrossRefGoogle Scholar
  17. Goto K, Oda H, Kondo H, Igaki M, Suzuki A, Tsuchiya S, Murase T, Hase T, Fujiya H, Matsumoto I, Naito H, Sugiura T, Ohira Y, Yoshioka T (2011) Responses of muscle mass, strength and gene transcripts to long-term heat stress in healthy human subjects. Eur J Appl Physiol 111:17–27CrossRefGoogle Scholar
  18. Hedgecock D, Lin JZ, DeCola S, Haudenschild CD, Meyer E, Manahan DT, Bowen B (2007) Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc Natl Acad Sci U S A 104:2313–2318CrossRefGoogle Scholar
  19. Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952CrossRefGoogle Scholar
  20. Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MAS, Lacy RC, Dasmahapatra KK (2014) High-throughput sequencing reveals inbreeding depression in a natural population. Proc Natl Acad Sci U S A 111:3775–3780CrossRefGoogle Scholar
  21. Hoffmann AA, Sgro CM, Kristensen TN (2017) Revisiting adaptive potential, population size, and conservation. Trends Ecol Evol 32:506–517CrossRefGoogle Scholar
  22. Hong HQ, Lu J, Fang XL, Zhang YH, Cai Y, Yuan J, Liu PQ, Ye JT (2018) G3BP2 is involved in isoproterenol-induced cardiac hypertrophy through activating the NF-kappaB signaling pathway. Acta Pharmacol Sin 39:184–194CrossRefGoogle Scholar
  23. Janicke T, Vellnow N, Lamy T, Chapuis E, David P (2014) Inbreeding depression of mating behavior and its reproductive consequences in a freshwater snail. Behav Ecol 25:288–299CrossRefGoogle Scholar
  24. Kardos M, Taylor HR, Ellegren H, Luikart G, Allendorf FW (2016) Genomics advances the study of inbreeding depression in the wild. Evol Appl 9:1205–1218CrossRefGoogle Scholar
  25. Lamas O, Moreno-Aliaga MJ, Martinez JA, Marti A (2003) NF-kappa B-binding activity in an animal diet-induced overweightness model and the impact of subsequent energy restriction. Biochem Biophys Res Commun 311:533–539CrossRefGoogle Scholar
  26. Lang RP, Bayne CJ, Camara MD, Cunningham C, Jenny MJ, Langdon CJ (2009) Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. Mar Biotechnol 11:650–668CrossRefGoogle Scholar
  27. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559CrossRefGoogle Scholar
  28. Lee HC, Chang DE, Yeom M, Kim GH, Choi KD, Shim I, Lee HJ, Hahm DH (2005) Gene expression profiling in hypothalamus of immobilization-stressed mouse using cDNA microarray. Mol Brain Res 135:293–300CrossRefGoogle Scholar
  29. Li Q, Xu K, Yu R (2007) Genetic variation in Chinese hatchery populations of the Japanese scallop (Patinopecten yessoensis) inferred from microsatellite data. Aquaculture 269:211–219CrossRefGoogle Scholar
  30. Li RJ, Zhang R, Zhang L, Zou JJ, Xing Q, Dou HQ et al (2015) Characterizations and expression analyses of NF-kappaB and Rel genes in the yesso scallop (Patinopecten yessoensis) suggest specific response patterns against gram-negative infection in bivalves. Fish Shellfish Immunol 44:611–621CrossRefGoogle Scholar
  31. Li SL, Li ZQ, Chen NS, Jin PF, Zhang JC (2019) Dietary lipid and carbohydrate interactions: implications on growth performance, feed utilization and non-specific immunity in hybrid grouper (Epinephelus fuscoguttatus female x E-lanceolatus male). Aquaculture 498:568–577CrossRefGoogle Scholar
  32. Liao W, Reed DH (2009) Inbreeding-environment interactions increase extinction risk. Anim Conserv 12:54–61CrossRefGoogle Scholar
  33. Liu Y, Xu C, Tang XB, Pei SR, Jin D, Guo MH et al (2018) Genomic methylation and transcriptomic profiling provides insights into heading depression in inbred Brassica rapa L. ssp pekinensis. Gene 665:119–126CrossRefGoogle Scholar
  34. Menzel M, Sletvold N, Agren J, Hansson B (2015) Inbreeding affects gene expression differently in two self-incompatible Arabidopsis lyrata populations with similar levels of inbreeding depression. Mol Biol Evol 32:2036–2047CrossRefGoogle Scholar
  35. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185CrossRefGoogle Scholar
  36. Murphy S, Zweyer M, Henry M, Meleady P, Mundegar RR, Swandulla D, Ohlendieck K (2018) Subproteomic profiling of sarcolemma from dystrophic mdx-4cv skeletal muscle. Data Brief 17:980–993CrossRefGoogle Scholar
  37. Nascimento-Sales M, Fredo-da-Costa I, Borges Mendes ACB, Melo S, Ravache TT, Gomez TGB, Gaisler-Silva F, Ribeiro MO, Santos AR Jr, Carneiro-Ramos MS, Christoffolete MA (2017) Is the FVB/N mouse strain truly resistant to diet-induced obesity? Physiol Rep 5:e13271CrossRefGoogle Scholar
  38. Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98CrossRefGoogle Scholar
  39. Pérez HM, Janssoone X, Nadeau M, Guderley H (2008) Force production during escape responses by Placopecten magellanicus is a sensitive indicator of handling stress: comparison with adductor muscle adenylate energy charge and phosphoarginine levels. Aquaculture 282:142–146CrossRefGoogle Scholar
  40. Phillippi AL, Yund PO (2017) Self-fertilization and inbreeding depression in three ascidian species that differ in genetic dispersal potential. Mar Biol 164:179Google Scholar
  41. Plough LV (2012) Environmental stress increases selection against and dominance of deleterious mutations in inbred families of the Pacific oyster Crassostrea gigas. Mol Ecol 21:3974–3987CrossRefGoogle Scholar
  42. Plough LV, Hedgecock D (2011) Quantitative trait locus analysis of stage-specific inbreeding depression in the Pacific oyster Crassostrea gigas. Genetics 189:1473–1486CrossRefGoogle Scholar
  43. Ponomarev I, Wang S, Zhang LL, Harris RA, Mayfield RD (2012) Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence. J Neurosci 32:1884–1897Google Scholar
  44. Reed DH, Fox CW, Enders LS, Kristensen TN (2012) Inbreeding-stress interactions: evolutionary and conservation consequences. Year Evol Biol 1256:33–48Google Scholar
  45. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140CrossRefGoogle Scholar
  46. Rosche C, Hensen I, Lachmuth S (2018) Local pre-adaptation to disturbance and inbreeding-environment interactions affect colonisation abilities of diploid and tetraploid Centaurea stoebe. Plant Biol 20:75–84CrossRefGoogle Scholar
  47. Schou MF, Loeschcke V, Kristensen TN (2015) Inbreeding depression across a nutritional stress continuum. Heredity 115:56–62CrossRefGoogle Scholar
  48. Schou MF, Bechsgaard J, Munoz J, Kristensen TN (2018) Genome-wide regulatory deterioration impedes adaptive responses to stress in inbred populations of Drosophila melanogaster. Evolution 72:1614–1628CrossRefGoogle Scholar
  49. Schrieber K, Lachmuth S (2017) The genetic paradox of invasions revisited: the potential role of inbreeding x environment interactions in invasion success. Biol Rev 92:939–952CrossRefGoogle Scholar
  50. Venney CJ, Johansson ML, Heath DD (2016) Inbreeding effects on gene-specific DNA methylation among tissues of Chinook salmon. Mol Ecol 25:4521–4533CrossRefGoogle Scholar
  51. Wang PZ, Guo JH, Wang F, Shi TP, Ma DL (2011) Human SBK1 is dysregulated in multiple cancers and promotes survival of ovary cancer SK-OV-3 cells. Mol Biol Rep 38:3551–3559CrossRefGoogle Scholar
  52. Wang W, Hui JHL, Chan TF, Chu KH (2014) De novo transcriptome sequencing of the snail Echinolittorina malaccana: identification of genes responsive to thermal stress and development of genetic markers for population studies. Mar Biotechnol 16:547–559CrossRefGoogle Scholar
  53. Wang S, Zhang JB, Jiao WQ, Li J, Xun XG, Sun Y et al (2017) Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol 1:120Google Scholar
  54. Wei G, Tao Y, Liu GZ, Chen C, Luo RY, Xia HA et al (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci U S A 106:7695–7701CrossRefGoogle Scholar
  55. Yadetie F, Oveland E, Doskeland A, Berven F, Goksoyr A, Karlsen OA (2017) Quantitative proteomics analysis reveals perturbation of lipid metabolic pathways in the liver of Atlantic cod (Gadus morhua) treated with PCB 153. Aquat Toxicol 185:19–28CrossRefGoogle Scholar
  56. Yan LL, Su JQ, Wang ZP, Zhang YH, Yan XW, Yu RH (2018) Growth performance and biochemical composition of the oysters Crassostrea sikamea, Crassostrea angulata and their hybrids in southern China. Aquac Res 49:1020–1028CrossRefGoogle Scholar
  57. Yang H, Wang XC, Wei YX, Deng Z, Liu H, Chen JS et al (2018) Transcriptomic analyses reveal molecular mechanisms underlying growth heterosis and weakness of rubber tree seedlings. BMC Plant Biol 18:10CrossRefGoogle Scholar
  58. Zajitschek SRK, Brooks RC (2010) Inbreeding depression in male traits and preference for outbred males in Poecilia reticulata. Behav Ecol 21:884–891CrossRefGoogle Scholar
  59. Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4.  https://doi.org/10.2202/1544-6115.1128
  60. Zhang LL, Hou R, Su HL, Hu XL, Wang S, Bao ZM (2012) Network analysis of oyster transcriptome revealed a cascade of cellular responses during recovery after heat shock. PLoS One 7:e35484CrossRefGoogle Scholar
  61. Zhao C, Sun P, Wei J, Zhang LS, Zhang WJ, Song J et al (2016) Larval size and metamorphosis are significantly reduced in second generation of inbred sea urchins Strongylocentrotus intermedius. Aquaculture 452:402–406CrossRefGoogle Scholar
  62. Zheng HP, Li L, Zhang GF (2012) Inbreeding depression for fitness-related traits and purging the genetic load in the hermaphroditic bay scallop Argopecten irradians irradians (Mollusca: Bivalvia). Aquaculture 366:27–33CrossRefGoogle Scholar
  63. Zhou T, Yuan ZH, Tan SX, Jin YL, Yang YJ, Shi HT et al (2018) A review of molecular responses of catfish to bacterial diseases and abiotic stresses. Front Physiol 9:1113Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Marine Genetics and Breeding (Ministry of Education)Ocean University of ChinaQingdaoChina
  2. 2.Laboratory for Marine Fisheries Science and Food Production ProcessesQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

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