Transcriptional Differences in Peanut (Arachis hypogaea L.) Seeds at the Freshly Harvested, After-ripening and Newly Germinated Seed Stages: Insights into the Regulatory Networks of Seed Dormancy Release and Germination

English version

Autoři: Pingli Xu ^aff001; Guiying Tang ^aff001; Weipei Cui ^aff001; Guangxia Chen ^aff003; Chang-Le Ma ^aff002; Jieqiong Zhu ^aff001; Pengxiang Li ^aff001; Lei Shan ^aff001; Zhanji Liu ^aff004; Shubo Wan ^aff001
Působiště autorů: Bio-Tech Research Center, Shandong Academy of Agricultural Sciences / Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Jinan, Shandong, China ^aff001; College of Life Science, Shandong Normal University, Jinan, Shandong, China ^aff002; Shandong Academy of Grape, Jinan, Shandong, China ^aff003; Shandong Cotton Research Center, Shandong Academy of Agricultural Sciences, Jinan, Shandong, China ^aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0219413

Souhrn

Seed dormancy and germination are the two important traits related to plant survival, reproduction and crop yield. To understand the regulatory mechanisms of these traits, it is crucial to clarify which genes or pathways participate in the regulation of these processes. However, little information is available on seed dormancy and germination in peanut. In this study, seeds of the variety Luhua No.14, which undergoes nondeep dormancy, were selected, and their transcriptional changes at three different developmental stages, the freshly harvested seed (FS), the after-ripening seed (DS) and the newly germinated seed (GS) stages, were investigated by comparative transcriptomic analysis. The results showed that genes with increased transcription in the DS vs FS comparison were overrepresented for oxidative phosphorylation, the glycolysis pathway and the tricarboxylic acid (TCA) cycle, suggesting that after a period of dry storage, the intermediates stored in the dry seeds were rapidly mobilized by glycolysis, the TCA cycle, the glyoxylate cycle, etc.; the electron transport chain accompanied by respiration was reactivated to provide ATP for the mobilization of other reserves and for seed germination. In the GS vs DS pairwise comparison, dozens of the upregulated genes were related to plant hormone biosynthesis and signal transduction, including the majority of components involved in the auxin signal pathway, brassinosteroid biosynthesis and signal transduction as well as some GA and ABA signal transduction genes. During seed germination, the expression of some EXPANSIN and XYLOGLUCAN ENDOTRANSGLYCOSYLASE genes was also significantly enhanced. To investigate the effects of different hormones during seed germination, the contents and differential distribution of ABA, GAs, BRs and IAA in the cotyledons, hypocotyls and radicles, and plumules of three seed sections at different developmental stages were also investigated. Combined with previous data in other species, it was suggested that the coordination of multiple hormone signal transduction nets plays a key role in radicle protrusion and seed germination.

Klíčová slova:

Gene expression – Signal transduction – Seeds – Seed germination – Peanut – Plant hormones – Auxins – Dehydrogenases

Zdroje

1. Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ. Molecular mechanisms of seed dormancy. Plant Cell Environ 2012; 35 : 1769–1786. doi: 10.1111/j.1365-3040.2012.02542.x 22620982

2. Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, et al. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J 2008; 53 : 214–224. doi: 10.1111/j.1365-313X.2007.03331.x 18028281

3. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D. Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 2005; 138 : 790–802. doi: 10.1104/pp.105.062778 15908592

4. Oracz K, El-MaaroufBouteau H, Farrant JM, Cooper K, Belghazi M, Job C, et al. ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 2007; 50 : 452–465. doi: 10.1111/j.1365-313X.2007.03063.x 17376157

5. Muller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G. The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol 2009; 184 : 885–897. doi: 10.1111/j.1469-8137.2009.03005.x 19761445

6. Fait A, Angelovici R, Less H, Ohad I, Urbanczyk-Wochniak E, Fernie AR, et al. Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol 2006; 142 : 839–854. doi: 10.1104/pp.106.086694 16963520

7. Finch-Savage WE, Leubner-Metzger G. Seed dormancy and the control of germination. New Phytol 2006; 171 : 501–523. doi: 10.1111/j.1469-8137.2006.01787.x 16866955

8. Muller K, Tintelnot S, Leubner-Metzger G. Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 2006; 47 : 864–877. doi: 10.1093/pcp/pcj059 16705010

9. Xi W, Liu C, Hou X, Yu H. MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 2010; 22 : 1733–1748. doi: 10.1105/tpc.109.073072 20551347

10. Ali-Rachedi S, Bouinot D, Wagner MH, Bonnet M, Sotta B, Grappin P, et al. Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta 2004; 219 : 479–488. doi: 10.1007/s00425-004-1251-4 15060827

11. Kucera B, Cohn MA, Leubner-Metzger G. Plant hormone interactions during seed dormancy release and germination. Seed Science Research 2005; 15 : 281–307. doi: 10.1079/ssr2005218

12. Hu Y, Yu D. BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant Cell 2014; 26 : 4394–4408. doi: 10.1105/tpc.114.130849 25415975

13. Wei T, He Z, Tan X, Liu X, Yuan X, Luo Y, et al. An integrated RNA-Seq and network study reveals a complex regulation process of rice embryo during seed germination. Biochem Biophys Res Commun 2015; 464 : 176–181. doi: 10.1016/j.bbrc.2015.06.110 26116530

14. Chen YT, Liu H, Stone S, Callis J. ABA and the ubiquitin E3 ligase KEEP ON GOING affect proteolysis of the Arabidopsis thaliana transcription factors ABF1 and ABF3. Plant J 2013; 75 : 965–976. doi: 10.1111/tpj.12259 23742014

15. Dekkers BJ, Pearce SP, van Bolderen-Veldkamp RP, Holdsworth MJ, Bentsink L. Dormant and after-ripened Arabidopsis thaliana seeds are distinguished by early transcriptional differences in the imbibed state. Front Plant Sci 2016; 7 : 1323. doi: 10.3389/fpls.2016.01323 27625677

16. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH. AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 2003; 17 : 410–418. doi: 10.1101/gad.1055803 12569131

17. Matakiadis T, Alboresi A, Jikumaru Y, Tatematsu K, Pichon O, Renou JP, et al. The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiol 2009; 149 : 949–960. doi: 10.1104/pp.108.126938 19074630

18. Nelson SK, Ariizumi T, Steber CM. Biology in the Dry Seed: Transcriptome changes associated with dry seed dormancy and dormancy loss in the Arabidopsis GA-insensitive sleepy1-2 mutant. Front Plant Sci 2017; 8 : 2158. doi: 10.3389/fpls.2017.02158 29312402

19. Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, et al. ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 2013; 9: e1003577. doi: 10.1371/journal.pgen.1003577 23818868

20. Sun TP. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 2011; 21: R338–345. doi: 10.1016/j.cub.2011.02.036 21549956

21. Wang Z, Ji H, Yuan B, Wang S, Su C, Yao B, et al. ABA signalling is fine-tuned by antagonistic HAB1 variants. Nat Commun 2015; 6 : 8138. doi: 10.1038/ncomms9138 26419884

22. Zhang X, Garreton V, Chua NH. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 2005; 19 : 1532–1543. doi: 10.1101/gad.1318705 15998807

23. Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T, Krasnogor N, et al. Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 2011; 108 : 9709–9714. doi: 10.1073/pnas.1100958108 21593420

24. Cao D, Xu H, Zhao Y, Deng X, Liu Y, Soppe WJ, et al. Transcriptome and degradome sequencing reveals dormancy mechanisms of Cunninghamia lanceolata seeds. Plant Physiol 2016; 172 : 2347–2362. doi: 10.1104/pp.16.00384 27760880

25. Dekkers BJ, Pearce S, van Bolderen-Veldkamp RP, Marshall A, Widera P, Gilbert J, et al. Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiol 2013; 163 : 205–215. doi: 10.1104/pp.113.223511 23858430

26. Bellieny-Rabelo D, De Oliveira EA, Ribeiro ES, Costa EP, Oliveira AE, Venancio TM. Transcriptome analysis uncovers key regulatory and metabolic aspects of soybean embryonic axes during germination. Sci Rep 2016; 6 : 36009. doi: 10.1038/srep36009 27824062

27. Issa F, Daniel F, Jean-Francois R, Hodo-Abolo T, Ndoye SM, Tahir DA, et al. Inheritance of fresh seed dormancy in Spanish-type peanut (Arachis hypogeea L.): bias introduced by inadvertent selfed flowers as revealed by microsatellite markers control. Afr. J. Biotechnol. 2010; 9 : 1905–1910. doi: 10.5897/AJB09.1321

28. Chen G, Shan L, Zhou LX, Tang GY, Bi YP. The comparison of different methods for isolating total RNA from peanuts. Chinese Agricultural Science Bulletin 2011; 27(1):214–218.(In Chinese)

29. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010; 28 : 511–515. doi: 10.1038/nbt.1621 20436464

30. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R STAT SOC B 1995; 57 : 289–300.

31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25 : 402–408. doi: 10.1006/meth.2001.1262 11846609

32. Yang J, Zhang J, Wang Z, Zhu Q, Wang W. Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 2001; 127 : 315–323. doi: 10.1104/pp.127.1.315 11553759

33. Weiler EW, Jourdan PS, Conrad W. Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 1981; 153 : 561–571. doi: 10.1007/BF00385542 24275876

34. Catusse J, Strub JM, Job C, Van Dorsselaer A, Job D. Proteome-wide characterization of sugarbeet seed vigor and its tissue specific expression. Proc Natl Acad Sci U S A 2008; 105 : 10262–10267. doi: 10.1073/pnas.0800585105 18635686

35. Holdsworth MJ, Bentsink L, Soppe WJ. Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 2008; 179 : 33–54. doi: 10.1111/j.1469-8137.2008.02437.x 18422904

36. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D. The effect of alpha-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 2004; 134 : 1598–1613. doi: 10.1104/pp.103.036293 15047896

37. Weitbrecht K, Muller K, Leubner-Metzger G. First off the mark: early seed germination. J Exp Bot 2011; 62 : 3289–3309. doi: 10.1093/jxb/err030 21430292

38. Buchanan BB, Gruissem W, Jones RL. Biochemistry & Molecular Biology of Plants. Rockville, Maryland, USA: American Society of Plant Physiologists. 2000; p679–687.

39. Frugis G, Chua NH. Ubiquitin-mediated proteolysis in plant hormone signal transduction. Trends Cell Biol 2002; 12 : 308–311. doi: 10.1016/s0962-8924(02)02308-5 12185846

40. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S. Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 2003; 15 : 1591–1604. doi: 10.1105/tpc.011650 12837949

41. Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, et al. Seed after-ripening is a discrete development pathway associated with specific gene networks in Arabidopsis. Plant J 2008; 53 : 214–224. doi: 10.1111/j.1365-313X.2007.03331.x 18028281

42. Cadman CS, Toorop PE, Hilhorst HW, Finch-Savage WE. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J 2006; 46 : 805–822. doi: 10.1111/j.1365-313X.2006.02738.x 16709196

43. Gao F, Jordan MC, Ayele BT. Transcriptional programs regulating seed dormancy and its release by after-ripening in common wheat (Triticumae stivum L.). Plant Biotechnol J 2012; 10 : 465–476. doi: 10.1111/j.1467-7652.2012.00682.x 22292455

44. Meimoun P, Mordret E, Langlade NB, Balzergue S, Arribat S, Bailly C, et al. Is gene transcription involved in seed dry after-ripening? PLoS One 2014; 9: e86442. doi: 10.1371/journal.pone.0086442 24466101

45. Chitnis VR, Gao F, Yao Z, Jordan MC, Park S, Ayele BT. After-ripening induced transcriptional changes of hormonal genes in wheat seeds: the cases of brassinosteroids, ethylene, cytokinin and salicylic acid. PLoS One 2014; 9: e87543. doi: 10.1371/journal.pone.0087543 24498132

46. Kermode AR. Role of abscisic acid in seed dormancy. Journal of Plant Growth Regulation 2005; 24 : 319–344. doi: 10.1007/s00344-005-0110-2

47. Finkelstein R, Reeves W, Ariizumi T, Steber C. Molecular aspects of seed dormancy. Annu Rev Plant Biol 2008; 59 : 387–415. doi: 10.1146/annurev.arplant.59.032607.092740 18257711

48. Wang Y, and Deng D. Molecular basis and evolutionary pattern of GA–GID1–DELLA regulatory module. Mol Genet Genomics 2014; 289 : 1–9. doi: 10.1007/s00438-013-0797-x 24322346

49. Chen F, Dahal P, Bradford KJ. Two Tomato expansin genes show divergent expression and localization in embryos during seed development and germination. Plant Physiol 2001; 127 : 928–936. doi: 10.1104/pp.010259 11706175

50. Chen F, Nonogaki H, Bradford KJ. A gibberellin-regulated xyloglucanendo transglycosylase gene is expressed in the endosperm cap during tomato seed germination. J Exp Bot 2002; 53 : 215–223. doi: 10.1093/jexbot/53.367.215 11807125

51. Marowa P, Ding A, Kong Y. Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Rep 2016; 35 : 949–965. doi: 10.1007/s00299-016-1948-4 26888755

52. Yan A, Wu M, Yan L, Hu R, Ali I, Gan Y. AtEXP2 is involved in seed germination and abiotic stress response in Arabidopsis. PLoS One 2014; 9: e85208. doi: 10.1371/journal.pone.0085208 24404203

53. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S. Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 2002; 130 : 1319–1334. doi: 10.1104/pp.011254 12427998

54. Leubner-Metzger G. Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways. Planta 2001; 213 : 758–763. doi: 10.1007/s004250100542 11678280

55. Kim TW, Wang ZY. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 2010; 61 : 681–704. doi: 10.1146/annurev.arplant.043008.092057 20192752

56. Nie S, Huang S, Wang S, Cheng D, Liu J, Lv S, et al. Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Front Plant Sci 2017; 8 : 1386. doi: 10.3389/fpls.2017.01386 28848587

57. Steber CM, McCourt P. A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 2001; 125 : 763–769. doi: 10.1104/pp.125.2.763 11161033

58. Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 2014; 3. doi: 10.7554/eLife.03031 24867218

59. Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 2004; 134 : 1555–1573. doi: 10.1104/pp.103.034736 15047898

60. Liu Y, Muller K, El-Kassaby YA, Kermode AR. Changes in hormone flux and signaling in white spruce (Picea glauca) seeds during the transition from dormancy to germination in response to temperature cues. BMC Plant Biol 2015; 15 : 292. doi: 10.1186/s12870-015-0638-7 26680643

61. Chapman EJ, Estelle M. Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 2009; 43 : 265–285. doi: 10.1146/annurev-genet-102108-134148 19686081

62. An ND, Wang LJ, Ding HC, Xu ZH. Auxin distribution and transport during embryogenesis and seed germination of Arabidopsis. Cell Research 2001; 11 : 273–278. doi: 10.1038/sj.cr.7290096 11787772

63. Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, et al. Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 2013; 197 : 1130–1141. doi: 10.1111/nph.12092 23252740

64. Nemhauser JL, Mockler TC, Chory J. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2004; 2: E258. doi: 10.1371/journal.pbio.0020258 15328536

65. Walcher CL, Nemhauser JL. Bipartite promoter element required for auxin response. Plant Physiol 2012; 158 : 273–282. doi: 10.1104/pp.111.187559 22100645

Článek Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna

Článek Evaluation of rice wild relatives as a source of traits for adaptation to iron toxicity and enhanced grain quality

Článek In vivo elongation of thin filaments results in heart failure

Článek Risk factors for third-generation cephalosporin resistant Enterobacteriaceae in gestational urine cultures: A retrospective cohort study based on centralized electronic health records

Článek Residential neighbourhood greenspace is associated with reduced risk of cardiovascular disease: A prospective cohort study

Článek Carotid plaques and neurological impairment in patients with acute cerebral infarction

Článek Modelling of amino acid turnover in the horse during training and racing: A basis for developing a novel supplementation strategy

Článek Trends of litter decomposition and soil organic matter stocks across forested swamp environments of the southeastern US

Článek Plasma proteome profiling of freshwater and seawater life stages of rainbow trout (Oncorhynchus mykiss)

Článek Link-centric analysis of variation by demographics in mobile phone communication patterns

Článek Lateral pressure equalisation as a principle for designing support surfaces to prevent deep tissue pressure ulcers

Článek Development of a risk score for prediction of poor treatment outcomes among patients with multidrug-resistant tuberculosis