Comparative analysis of the accelerated aged seed transcriptome profiles of two maize chromosome segment substitution lines

Autoři: Li Li aff001;  Feng Wang aff001;  Xuhui Li aff001;  Yixuan Peng aff001;  Hongwei Zhang aff002;  Stefan Hey aff003;  Guoying Wang aff002;  Jianhua Wang aff001;  Riliang Gu aff001
Působiště autorů: Seed Science and Technology Research Center, Beijing Innovation Center for Seed Technology (MOA), Beijing Key Laboratory for Crop Genetic Improvement, College of Agronomy and Biotechnology, China Agricultural University, Beijing, China aff001;  Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China aff002;  Department of Agronomy, Iowa State University, Ames, Iowa, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0216977


Seed longevity is one of the most essential characteristics of seed quality. Two chromosome segment substitution lines, I178 and X178, which show significant differences in seed longevity, were subjected to transcriptome sequencing before and after five days of accelerated aging (AA) treatments. Compared to the non-aging treatment, 286 and 220 differentially expressed genes (DEGs) were identified after 5 days of aging treatment in I178 and X178, respectively. Of these DEGs, 98 were detected in both I178 and X178, which were enriched in Gene Ontology (GO) terms of the cellular component of the nuclear part, intracellular part, organelle and membrane. Only 86 commonly downregulated genes were enriched in GO terms of the carbohydrate derivative catabolic process. Additionally, transcriptome analysis of alternative splicing (AS) events in I178 and X178 showed that 63.6% of transcript isoforms occurred AS in all samples, and only 1.6% of transcript isoforms contained 169 genes that exhibited aging-specific AS arising after aging treatment. Combined with the reported QTL mapping result, 7 DEGs exhibited AS after aging treatment, and 13 DEGs in mapping interval were potential candidates that were directly or indirectly related to seed longevity.

Klíčová slova:

Carbohydrates – Energy metabolism – Gene expression – Maize – Nutrient and storage proteins – Seed germination – Seeds – Intracellular membranes


1. Agacka-Moldoch M, Nagel M, Doroszewska T, Lewis RS, Börne A. Mapping quantitative trait loci determining seed longevity in tobacco (Nicotiana tabacum L.). Euphytica. 2015; 202(3): 479–486.

2. Walters C. Understanding the mechanisms and kinetics of seed ageing. Seed Sci. Res. 1998; 8: 223–244.

3. Groot S, Surki A, Vos R and Kodde J. Seed storage at elevated partial pressure of oxygen, a fast method for analysing seed ageing under dry conditions. Ann. Bot. 2012; 110: 1149–1159. doi: 10.1093/aob/mcs198 22967856

4. Xin X, Lin X, Zhou Y, Chen X, Liu X, Lu X. Proteome analysis of maize seeds: the effect of artificial ageing. Physiol. Plantarum. 2011; 143, 126–138.

5. Xin X, Tian Q, Yin G, Chen X, Zhang J, Ng S. Reduced mitochondrial and ascorbate-glutathione activity after artificial ageing in soybean seed. J. Plant Physiol. 2014; 171, 140–147. doi: 10.1016/j.jplph.2013.09.016 24331429

6. Nguyen TP, Cueff G, Hegedus DD, Rajjou L, Bentsink L. A role for seed storage proteins in Arabidopsis seed longevity. J. Exp. Bot. 2015; 66, 6399–6413. doi: 10.1093/jxb/erv348 26184996

7. Yin G, Xin X, Fu S, An M, Wu S, Chen X, Zhang J, He J, Whelan J, Lu X. Proteomic and carbonylation profile analysis at the critical node of seed ageing in oryza sativa. Sci. Rep. 2017; 7, 1–12. doi: 10.1038/s41598-016-0028-x

8. He Y, Cheng J, Li X. Acquisition of desiccation tolerance during seed development is associated with oxidative processes in rice. Botanique. 2015; 94(2): 91–101.

9. Debeaujon I, Leon-Kloosterziel KM, Koornneef M. Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 2000; 122(2): 403–414 doi: 10.1104/pp.122.2.403 10677433

10. Murthy UMN, Kumar PP, Sun WQ. Mechanisms of seed ageing under different storage conditions for Vigna radiata (L.) Wilczek: lipid peroxidation, sugar hydrolysis, Maillard reactions and their relationship to glass state transition. J Exp Bot. 2003; 54(384): 1057–1067. doi: 10.1093/jxb/erg092 12598575

11. Zhan J, Li W, He HY, Li CZ, He LF. Mitochondrial alterations during Al-induced PCD in peanut root tips. Plant Physiol Biochem. 2014; 75:105–113. doi: 10.1016/j.plaphy.2013.12.010 24398246

12. Yin G, Whelan J, Wu S, Zhou J, Chen B, Chen X, Zhang J, He J, Xin X, Lu X. Comprehensive mitochondrial metabolic shift during the critical node of seed ageing in rice. PLoS One. 2016; 11, e0148013. doi: 10.1371/journal.pone.0148013 27124767

13. Sano N, Kim JS, Onda Y, Nomura T, Mochida K. Okamoto M, Seo M. RNA-Seq using bulked recombinant inbred line populations uncovers the importance of brassinosteroid for seed longevity after priming treatments. Scientific report. 2017; 7: 8095 doi: 10.1038/s41598-017-08116-5

14. Lv Y, Zhang S, Wang J, Hu Y. Quantitative Proteomic Analysis of Wheat Seeds during Artificial Ageing and Priming Using the Isobaric Tandem Mass Tag Labeling. PLOS ONE. 2016; doi: 10.1371/journal.pone.0162851 September 15, 2016 27632285

15. Wang W, Liu S, Song S, Møller IM. Proteomics of seed development, desiccation tolerance, germination and vigor. Plant Physiol. Biochem. 2015; 86, 1–15. doi: 10.1016/j.plaphy.2014.11.003 25461695

16. Chen X, Yin G, Börnerb A, Xin X, He J, Nage M, Liu X, Lu X. Comparative physiology and proteomics of two wheat genotypes differing in seed storage tolerance. Plant Physiology and Biochemistry. 2018; 130:455–463. doi: 10.1016/j.plaphy.2018.07.022 30077921

17. Liu Y, Zhang H, Li X, Wang F, Lyle D, Sun L, Wang G, Wang J, Li L, Gu R. Quantitative trait locus mapping for seed artificial aging traits using an F2:3 population and a recombinant inbred line population crossed from two highly related maize inbreds. Plant Breeding. 2018; (138):29–37.

18. Wang G, Sun X, Wang G, Wang F, Gao Q, Sun X, Tang Y, Chang C, Lai J, Zhu L, Xu Z, Song R. Opaque7 encodes an acyl-activating enzyme-like protein that affects storage protein synthesis in maize endosperm. Genetics. 2011; 189: 1281–1295. doi: 10.1534/genetics.111.133967 21954158

19. International rules for seed test. International seed testing association (ISTA). Switzerland: Zurich. 2018; Chapter 15–6.

20. Barber RD, Harmer DW, Coleman RA, Clark BJ. GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol Genomics. 2005; 21:389–395 doi: 10.1152/physiolgenomics.00025.2005 15769908

21. Oliveros JC. VENNY. An interactive tool for comparing lists with Venn Diagrams. 2007;

22. Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z. AgriGO v2.0: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2017; 45(Web Server issue): W122–W129. doi: 10.1093/nar/gkx382 28472432

23. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004; 37:914–39. doi: 10.1111/j.1365-313x.2004.02016.x 14996223

24. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biol. 2010; 11, R14. doi: 10.1186/gb-2010-11-2-r14 20132535.

25. Shewry PR, Halford NG. Cereal seed storage proteins: Structures, properties and role in grain utilization. J Exp Bot. 2002; 53:947–958. doi: 10.1093/jexbot/53.370.947 11912237

26. Rajjou L, Miche L, Huguet R, Job C, Job D. The use of proteome and transcriptome profiling in the understanding of seed germination and identification of intrinsic markers determining seed quality, germination efficiency and early seedling vigour. In: Navie SC, Adkins SW, Ashmore S, eds. Seeds: Biology, Development and Ecology. Oxfordshire, CAB International, 2007; 149–158.

27. Rajjou J, Lovigny Y, et al. Proteome-Wide Characterization of Seed Aging in Arabidopsis: A Comparison between Artificial and Natural Aging Protocols. Plant Physiology. 2008; 148: 620–641. doi: 10.1104/pp.108.123141 18599647

28. Bewley JD. Seed germination and dormancy. Plant Cell. 1997; 9: 1055–1066. doi: 10.1105/tpc.9.7.1055 12237375

29. Sano N, Rajjou L, North HM, Debeaujon I, Marion-Poll A, Seo M. Staying Alive: Molecular Aspects of Seed Longevity. Plant Cell Physiol. 2016; 57(4):660–74. doi: 10.1093/pcp/pcv186 26637538

30. Petla BP, Kamble NU, Kumar M, Verma P, Ghosh S, Singh A, Rao V, Salvi P, Kaur H, Saxena SC, Majee M. Rice PROTEIN l-ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity. New Phytol. 2016; 211(2):627–45. doi: 10.1111/nph.13923 26987457

31. Ogunola OF, Hawkins LK, Mylroie E, Kolomiets MV, Borrego E, Tang JD, Williams WP, Warburton ML. Characterization of the maize lipoxygenase gene family in relation to aflatoxin accumulation resistance. PLoS One. 2017; 12(7):e0181265. eCollection 2017. doi: 10.1371/journal.pone.0181265 28715485

32. Li Z, Gao Y, Lin C, Pan R, Ma W, Zheng Y, Guan Y, Hu J. Suppression of LOX activity enhanced seed vigour and longevity of tobacco (Nicotiana tabacum L.) seeds during storage. Conserv Physiol. 2018; 6(00): coy047;

33. Mochizuki S, Sugimoto K, Koeduka T, Matsui K. Arabidopsis lipoxygenase 2 is essential for formation of green leaf volatiles and five-carbon volatiles. FEBS Lett. 2016; 590(7):1017–27. https://doi:10.1002/1873-3468.12133.

34. Charton L, Plett A, Linka N. Plant peroxisomal solute transporter proteins. J Integr Plant Biol. 2019; Accepted.

35. Mudgil Yashwanti, Shiu Shin-Han, Stone Sophia L., Salt Jennifer N., and Goring Daphne R. A Large Complement of the Predicted Arabidopsis ARM Repeat Proteins Are Members of the U-Box E3 Ubiquitin Ligase Family Plant Physiol. 2004; (134):59–66

36. Shen W, Yao X, Ye T, Ma S, Liu X, Yin X, Wu Y. Arabidopsis Aspartic Protease ASPG1 Affects Seed Dormancy, Seed Longevity and Seed Germination. Plant Cell Physiol. 2018; 59(7):1415–1431. doi: 10.1093/pcp/pcy070 29648652

37. Dinh SN and Kang H. An endoplasmic reticulum-localized Coffea arabica BURP domain-containing protein affects the response of transgenic Arabidopsis plants to diverse abiotic stresses. Plant Cell Rep. 2017; 36(11):1829–1839. doi: 10.1007/s00299-017-2197-x 28803325

38. Li Y, Chen X, Chen Z, Cai R, Zhang H, Xiang Y. Identification and Expression Analysis of BURP Domain-Containing Genes in Medicago truncatula. Front Plant Sci. 2016; 7:485. eCollection 2016. doi: 10.3389/fpls.2016.00485 27148311

39. Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol. 2010; 153(4):1526–38. doi: 10.1104/pp.110.157370 20566705

40. Chow LT, Gelinas RE, Broker TR, Roberts RJ. An amazing sequence arrangement at the 5’ends of adenovirus 2 messenger RNA. Cell. 1977; 12, 1–8. doi: 10.1016/0092-8674(77)90180-5 902310

41. Bush SJ, Chen L, Tovar-Corona JM, Urrutia AO. Alternative splicing and the evolution of phenotypic novelty. Philos Trans R Soc Lond B Biol Sci. 2017; 372(1713): 20150474. doi: 10.1098/rstb.2015.0474 27994117

42. Kim N, Alekseyenko AV, Roy M, Lee C. The ASAP II database: analysis and comparative genomics of alternative splicing in 15 animal species. Nucleic Acids Res. 2007; 35, D93–D98. doi: 10.1093/nar/gkl884 17108355

43. Grutzmann K, Szafranski K, Pohl M, Voigt K, Petzold A, Schuster S. Fungal alternative splicing is associated with multicellular complexity and virulence: a genome-wide multi-species study. DNA Res. 2014; 21, 27–39. doi: 10.1093/dnares/dst038 24122896

44. Zhang C, Yang H, Yang H. Evolutionary character of alternative splicing in plants. Bioinform. Biol. Insights. 2016; 9(Suppl 1), 47–52. eCollection 2015.

45. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 2008; 40, 1413–1415. doi: 10.1038/ng.259 18978789

46. Wang ET, Sandberg R, Luo SJ, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature. 2008; 456, 470–476. doi: 10.1038/nature07509 18978772

47. Matsushita K, Otofuji A, Iwahashi M, Toyama H, Adachi O. NADH dehydrogenase of Corynebacterium glutamicum. Purification of an NADH dehydrogenase II homolog able to oxidize NADPH. FEMS Microbiol Lett. 2001; 204 (2):271–6. doi: 10.1111/j.1574-6968.2001.tb10896.x 11731134

48. Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle M, Chory J. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 2001; 15(15):1985–97. doi: 10.1101/gad.905201 11485992

49. Desgagné-Penix I, Eakanunkul S, Coles JP, Phillips AL, Hedden P, Sponsel VM. The auxin transport inhibitor response 3 (tir3) allele of BIG and auxin transport inhibitors affect the gibberellin status of Arabidopsis. Plant J. 2005; 41(2):231–42. doi: 10.1111/j.1365-313X.2004.02287.x 15634200

50. Daloso DM, Williams TC, Antunes WC, Pinheiro DP, Müller C, Loureiro ME, Fernie AR. Guard cell-specific upregulation of sucrose synthase 3 reveals that the role of sucrose in stomatal function is primarily energetic. New Phytol. 2016; 209(4):1470–83. doi: 10.1111/nph.13704 26467445

51. Krishnan HB, Jang S, Kim WS, Kerley MS, Oliver MJ, Trick HN. Biofortification of soybean meal: immunological properties of the 27 kDa γ-zein. J Agric Food Chem. 2011; 59(4):1223–8. doi: 10.1021/jf103613s 21226519

Článek vyšel v časopise


2019 Číslo 11