Steady expression of high oleic acid in peanut bred by marker-assisted backcrossing for fatty acid desaturase mutant alleles and its effect on seed germination along with other seedling traits


Autoři: Sandip K. Bera aff001;  Jignesh H. Kamdar aff001;  Swati V. Kasundra aff001;  Sahil V. Patel aff001;  Mital D. Jasani aff001;  A. K. Maurya aff001;  P. Dash aff001;  Ajay B. Chandrashekar aff001;  Kirti Rani aff001;  N. Manivannan aff002;  Pasupuleti Janila aff003;  Manish K. Pandey aff003;  R. P. Vasanthi aff004;  K. L. Dobariya aff005;  T. Radhakrishnan aff001;  Rajeev K. Varshney aff003
Působiště autorů: Indian Council of Agricultural Research-Directorate of Groundnut Research (ICAR-DGR), Junagadh, India aff001;  National Pulses Research Center, Tamil Nadu Agricultural University (TNAU), Vamban Colony, Pudukkottai, Tamil Nadu, India aff002;  International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, India aff003;  Regional Agricultural Research Station, Acharya NG Ranga Agricultural University (ANGRAU), Tirupati, India aff004;  Main Oilseeds Research Station, Junagadh Agricultural University (JAU), Junagadh, India aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226252

Souhrn

Peanut (Arachis hypogaea L.) is an important nutrient-rich food legume and valued for its good quality cooking oil. The fatty acid content is the major determinant of the quality of the edible oil. The oils containing higher monounsaturated fatty acid are preferred for improved shelf life and potential health benefits. Therefore, a high oleic/linoleic fatty acid ratio is the target trait in an advanced breeding program. The two mutant alleles, ahFAD2A (on linkage group a09) and ahFAD2B (on linkage group b09) control fatty acid composition for higher oleic/linoleic ratio in peanut. In the present study, marker-assisted backcrossing was employed for the introgression of two FAD2 mutant alleles from SunOleic95R into the chromosome of ICGV06100, a high oil content peanut breeding line. In the marker-assisted backcrossing-introgression lines, a 97% increase in oleic acid, and a 92% reduction in linoleic acid content was observed in comparison to the recurrent parent. Besides, the oleic/linoleic ratio was increased to 25 with respect to the recurrent parent, which was only 1.2. The most significant outcome was the stable expression of oil-content, oleic acid, linoleic acid, and palmitic acid in the marker-assisted backcrossing-introgression lines over the locations. No significant difference was observed between high oleic and normal oleic in peanuts for seedling traits except germination percentage. In addition, marker-assisted backcrossing-introgression lines exhibited higher yield and resistance to foliar fungal diseases, i.e., late leaf spot and rust.

Klíčová slova:

Alleles – Fatty acids – Oils – Oleic acid – Peanut – Seed germination – Vegetable oils – Linoleic acid


Zdroje

1. FAOSTAT 2017 Available: http://faostat.fao.org accessed on 22-03-2019.

2. Kavera B, Nadaf HL, Hanchinal RR. Near infrared reflectance spectroscopy (NIRS) for large scale screening of fatty acid profile in peanut (Arachis hypogaea L.), Legume res. 2014; 37:272–280. doi: 10.5958/j.0976-0571.37.3.041

3. Johnson S, Saikia N. Fatty acids profile of edible oils and fat in India, Centre for Science and Environment, New Delhi, 2008; pp. 1–48.

4. Kratz M, Cullen P, Kannenberg F, Kassner A, Fobker M, Abuja PM, et al. Effects of dietary fatty acids on the composition and oxidizability of low density lipoprotein. European Journal of Clinical Nutrition. 2002; 56:72–81. doi: 10.1038/sj.ejcn.1601288 11840183

5. WHO. Diet, nutrition and the prevention of chronic diseases, WHO technical report series 916, Report of a joint WHO/FAO expert consultation, World Health Organization, Geneva. 2003; 88

6. Wang CT. Peanut production, trade and utilization Peanut Science and Technology Bulletin, National Peanut Agri-Indus Res Sys. 2009; 1 (5&6), 8–32.

7. Vassiliou EK, Gonzalez A, Garcia C, Tadros JH, Chakraborty G, Toney JH. Oleic acid and peanut oil high in oleic acid reverse the inhibitory effect of insulin production of the inflammatory cytokine TNF-alpha both in vitro and in vivo systems. Lipids in Health and Disease. 2009; 8:25. doi: 10.1186/1476-511X-8-25 19558671

8. O’Byrne DJ, Knauft DA, Shireman RB. Low fat-monounsaturated rich diets containing high-oleic peanuts improve serum lipoprotein profiles. Lipids. 1997; 32(7):687–695. doi: 10.1007/s11745-997-0088-y 9252956

9. Yamaki T, Nagamine I, Fukumoto K, Yano T, Miyahara M, Sakurai H. High oleic peanut oil modulates promotion stage in lung tumorigenesis of mice treated with methyl nitrosourea. Food Science and Technology Research. 2005; 11:231–235. https://doi.org/10.3136/fstr.11.231

10. O’keefe SF, Wiley VA, Knauft DA. Comparison of oxidative stability of high-and normal-oleic peanut oils. J Am Oil Chem Soc. 1993; 70(5):489–492. https://doi.org/10.1007/ BF02542581

11. Jung S, Powell G, Moore K, Abbott A. The high oleate trait in the cultivated peanut (Arachis hypogaea L.). II. Molecular basis and genetics of the trait. Mol Gen Genet. 2000b 263:806–811. doi: 10.1007/s004380000243 10905348

12. Lopez Y, Nadaf HL, Smith OD, Connell JP, Reddy AS, Fritz AK. Isolations and characterization of the Δ12 fatty acid desaturase in peanut (Arachis hypogaea L.) and search for polymorphism for the high oleate trait in Spanish market-type lines. Theor Appl Genet. 2000; 101:1131–1138. https://doi.org/10.1007/s001220051589

13. Chu Y, Holbrook CC, Ozias-Akins P. Two alleles of control the high oleic acid trait in cultivated peanut. Crop sci. 2009; 49:2029–2036. doi: 10.2135/cropsci2009.01.0021

14. Pandey MK, Wang ML, Qiao L, Feng S, Khera P, Wang H, et al. Identification of QTLs associated with peanut oil contents in RIL populations and mapping FAD2 genes and their relative contribution towards oil quality. BMC Genetics. 2014; 15:133. doi: 10.1186/s12863-014-0133-4 25491595

15. Jung S, Swift D, Sengoku E, Patel M, Teule F, Powell G, et al. The high oleate trait in the cultivated peanut (Arachis hypogaea L.) I. Isolation and characterization of two genes encoding microsomal oleoyl-PC desaturases. Mol Gen Genet. 2000a; 263:796–805. doi: 10.1007/s004380000244 10905347

16. Gorbet DW, Knauft DA. Registration of ‘SunOleic 95R’peanut. Crop sci. 1997; 37:1392.

17. Wang ML, Chen CY, Tonnis B, Barkley NA, Pinnow DL, Pittman RN, et al. Oil, fatty acid, flavonoid, and resveratrol content variability and FAD2A functional SNP genotypes in the US peanut mini-core collection. J Agric Food Chem. 2013; 61:2875–2882. doi: 10.1021/jf305208e 23379758

18. Wang ML, Khera P, Pandey MK, Wang H, Qiao L, Feng S, et al. Genetic mapping of QTLs controlling fatty acids provided insights into the genetic control of fatty acid synthesis pathway in peanut (Arachis hypogaea L.). PLoS One. 2015a; 10(4):e0119454. doi: 10.1371/journal.pone.0119454 25849082

19. Norden AJ, Gorbet DW, Knauft DA, Young CT. Variability in oil quality among peanut genotypes in the Florida breeding program. Peanut Sci. 1987; 14:7–11. https://doi.org/10.3146/i0095-3679-14-1-3

20. Chen Z, Wang ML, Barkley NA, Pittman RN. A simple allele-specific PCR assay for detecting FAD2 alleles in both A and B genomes of the cultivated peanut for high-oleate trait selection. Plant Mol Biol Rep. 2010; 28:542–548. https://doi.org/10.1007/s11105-010-0181-5

21. Chu Y, Ramos L, Holbrook CC, Ozias-Akins P. Frequency of a loss-of-function mutation in Oleoyl-PC Desaturase (ahFAD2A) in the mini-core of the US peanut germplasm collection. Crop sci. 2007; 47:2372–2378. 10.2135/cropsci2007.02.0117

22. Janila P, Pandey MK, Shasidhar Y, Variatha MT, Sriswathi M, Khera P, et al. Molecular breeding for introgression of fatty acid desaturase mutant alleles (ahFAD2A and ahFAD2B) enhances oil quality in high and low oil containing peanut genotypes. Plant Sci. 2016; 242:203–213. doi: 10.1016/j.plantsci.2015.08.013 26566838

23. Bera SK, Kamdar JH, Kasundra SV, Dash P, Maurya AK, Jasani MD, et al. Improving oil quality by altering levels of fatty acids through marker-assisted selection of ahfad2 alleles in peanut (Arachis hypogaea L.). Euphytica. 2018; 214:162. https://doi.org/10.1007/s10681-018-2241-0

24. Grosso NR, Lamarque A, Maestri D, Zygadlo J, Guzmán C. Fatty acid variation of runner peanut (Arachis hypogaea L.) among geographic localities from Cordoba (Argentina). J Am Oil Chem Soc. 1994; 71:541–542. https://doi.org/10.1007/BF02540669

25. Grosso N, Guzmán C. Chemical composition of aboriginal peanut (Arachis hypogaea L.) seeds from Peru. J Agric Food Chem. 1995; 43:102–105. doi: 10.1021/jf00049a019

26. Dwivedi SL, Nigam SN, Jambunathan R, Sahrawat KL, Nagabhushanam GVS, Raghunath K. Effect of genotypes and environments on oil content and oil quality parameters and their association in peanut (Arachis hypogaea L.). Peanut Sci. 1993; 20:84–89. https://doi.org/10.3146/i0095-3679-20-2-5

27. Andersen PC, Gorbet DW. Influence of year and planting date on fatty acid chemistry of high oleic acid and normal peanut genotypes. Journal of Agricultural and Food Chemistry. 2002; 50:1298–1305. doi: 10.1021/jf0113171 11853521

28. Sogut T, Ozturk F, Kizil S. Effect of sowing time on peanut (Arachis hypogaea L.) cultivars: i. yield, yield components, oil and protein content. Scientific Papers-Series A, Agronomy. 2016; 59: 415–420. doi: 10.1016/j.aaspro.2016.09.018

29. Chaiyadee S, Jogloy S, Songsri P, Singkham N, Vorasoot N, Sawatsitang P, et al. Soil moisture affects fatty acids and oil quality parameters in peanut. International Journal of Plant Production. 2013; 7:81–96.

30. Dwivedi SL, Nigam SN, Rao RN, Singh U, Rao KVS. Effect of drought on oil, fatty acids and protein contents of groundnut (Arachis hypogaea L.) seeds. Field crops research. 1996; 48(2–3):125–133. https://doi.org/10.1016/S0378-4290(96)01027-1

31. Golombek D, Sridhar R, Singh U. Effect of soil temperature on the seed composition of three Spanish cultivars of groundnut (Arachis hypogaea L.). J Agric Food Chem. 1995; 43:2067–2070. doi: 10.1021/jf00056a021

32. Li X, Wu L, Qiu G, Wang T, Liu C, Yang Y, et al. Effects of sowing season on agronomic traits and fatty acid metabolic profiling in three Brassica napus L. Cultivars. Metabolites. 2019; 9(2):37. https://doi.org/10.3390/metabo 9020037

33. Flagella Z, Rotunno T, Tarantino E, Di Caterina R, De Caro A. Changes in seed yield and oil fatty acid composition of high oleic sunflower (Helianthus annuus L.) hybrids in relation to the sowing date and the water regime. European journal of agronomy. 2002; 17(3):221–230. https://doi.org/10.1016/S1161-0301(02)00012-6

34. Copeland LO, McDonald MB. Seed vigor and vigor testing. In Principles of Seed Science and Technology.Springer, Boston, MA. 2001.

35. Sun M, Spears JF, Isleib TG, Jordan DL, Penny B, Johnson D, et al. Effect of production environment on seed quality of normal and high-oleate large seeded Virginia-type peanut (Arachis hypogaea L.). Peanut Sci. 2014; 41(2):90–99. https://doi.org/10.3146/PS12-16.1

36. Jungman BS, Schubert AM. The effect of fatty acid profiles on peanut seed germination at low soil temperatures. Proc Amer Peanut Res Educ Soc. 2000; 32:36.

37. Upadhyaya HD, Dwivedi SL, Vadez V, Hamidou F, Singh S, Varshney RK, et al. Multiple resistant and nutritionally dense germplasm identified from mini core collection in peanut. Crop Sci. 2014; 54(2): 679–693. doi: 10.2135/cropsci2013.07.0493

38. Nawade B, Bosamia TC, Thankappan R, Rathnakumar AL, Kumar A, Dobaria JR, et al. Insights into the Indian Peanut Genotypes for ahFAD2 Gene Polymorphism Regulating Its Oleic and Linoleic Acid Fluxes. Front. Plant Sci. 2016; 7:1271. doi: 10.3389/fpls.2016.01271 27610115

39. Mace ES, Buhariwalla KK, Buhariwalla HK, Crouch JH. A high-throughput DNA extraction protocol for tropical molecular breeding programs. Plant Mol Biol Rep. 2003; 21:459–460. https://doi.org/10.1007/BF02772596

40. Gautami B, Foncéka D, Pandey MK, Moretzsohn MC, Sujay V, Qin H, et al. An international reference consensus genetic map with 897 marker loci based on 11 mapping populations for tetraploid groundnut (Arachis hypogaea L.). PLoS One. 2012; 7:41213. https://doi.org/10.1371/journal.pone.0041213

41. Bera SK, Kamdar JH, Kasundra SV, Ajay BC. Identification of a novel QTL governing resistance to Sclerotial stem rot disease in peanut. Australasian Plant Pathology. 2016; 45: 637. doi: 10.1007/s133313-016-0448-x

42. Jokić S, Sudar R, Svilovic S, Vidović S, Bilić M, Velić D. Fatty Acid Composition of Oil Obtained from Soybeans by Extraction with Supercritical Carbon Dioxide. Czech J Food Sci. 2013; 31:116–125.

43. Kharb RPS, Lather BPS, Deswal DP. Prediction of Field Emergence through Heritability and Genetic Advance of Vigour Parameters. Seed Science and Technology. 1994; 22:461–466.

44. IBPGR & ICRISAT. Descriptors for groundnut, 125 International Board for Plant Genetic Resources, Rome, Italy and International Crops Research Institute for the Semi-Arid Tropics, Andhra Pradesh, India. 1992; ISBN 92-9043-139-3.

45. Vishwakarma MK, Mishra VK, Gupta PK, Yadav PS, Kumar H, Joshi AK. Introgression of the high grain protein gene Gpc-B1 in an elite wheat variety of Indo-Gangetic Plains through marker assisted backcross breeding. Current Plant Biology. 2014; 1:60–7.

46. R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. 2015.

47. IRRI. CropStat for Windows, Version 7.2, IRRI 2007.

48. Arya SS, Salve AR, Chauhan S. Peanuts as functional food: a review. J Food Sci Technol. 2016; 53:31–41. doi: 10.1007/s13197-015-2007-9 26787930

49. Pandey MK, Monyo E, Ozias-Akins P, Liang X, Guimarães P, Nigam SN, et al. Advances in Arachis genomics for peanut improvement. Biotechnology Advances. 2012; 30 (3): 639–651. doi: 10.1016/j.biotechadv.2011.11.001 22094114

50. Varshney RK, Mohan SM, Gaur PM, Gangarao NVPR, Pandey MK, Bohra A, et al. Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnology Advances. 2013; 31:1120–1134. doi: 10.1016/j.biotechadv.2013.01.001 23313999

51. Chu Y, Wu CL, Holbrook CC, Tillman BL, Person G, Ozias-Akins P. Marker-assisted selection to pyramid nematode resistance and the high oleic trait in peanut. Plant Genome. 2011; 4:110–117. doi: 10.3835/plantgenome2011.01.0001

52. Varshney RK, Pandey MK, Janila P, Nigam SN, Sudini H, Gowda MVC, et al. Marker-assisted introgression of a QTL region to improve rust resistance in three elite and popular varieties of peanut (Arachis hypogaea L.). Theor Appl Genet. 2014; 127:1771–1781. doi: 10.1007/s00122-014-2338-3 24927821

53. Wang XZ, Wu Q, Tang YY, Sun QX, Wang CT. FAD2B from a peanut mutant with high oleic acid content was not completely dysfunctional. Advances in Applied Biotechnology. 2015b; 332: 265–271. https://doi.org/10.1007/978-3-662-45657-6_28

54. Sarvamangala C, Gowda MVC, Varshney RK. Identification of quantitative trait loci for protein content, oil content and oil quality for groundnut (Arachis hypogaea L.). Field Crops Res. 2011; 122:49–59. https://doi.org/10.1016/j.fcr.2011.02.010

55. Mercer LC, Wynne TC, Young CT. Inheritance of fatty acid content in peanut oil. Peanut Sci. 1990; 17:17–21. https://doi.org/10.3146/i0095-3679-17-1-7

56. Gulluoglu L, Bakal H, Onat B, El Sabagh A, Arioglu H. Characterization of peanut (Arachis hypogaea L.) seed oil and fatty acids composition under different growing season under Mediterranean environment. Journal of Experimental Biology and Agricultural Sciences. 2016; 4(5S):564–571. http://dx.doi.org/10.18006/2016

57. Bansal UK, Satija DR, Ahula KL. Oil composition of diverse groundnut (Arachis hypogaea L.) genotypes relation to different environments. J Sci Food Agric. 1993; 63:17–19. https://doi.org/10.1002/jsfa.2740630104

58. Raheja RK, Battai SK, Ahuja KL, Labana KS, Singh M. Comparison of oil content and fatty acid composition of peanut genotypes differing in growth habit. Plant Food Hum Nutr. 1987; 37:103–108. doi: 10.1007/BF01092045

59. Hasan MM, Rafii MY, Ismail MR, Mahmood M, Rahim HA, Alam MA, et al. Marker-assisted backcrossing: a useful method for rice improvement. Biotechnology & Biotechnological Equipment. 2015; 29(2):237–254. doi: 10.1080/13102818.2014.995920

60. Marambe B, Nagaoka T, Anso T. Identification and biological activity of germination—inhibiting long-chain fatty acids in animal-waste composts. Plant Cell Physiol. 1993; 34, 605–612. 8025825

61. Vincenzini MT, Vincieri F, Vanni P. The effects of octanoate and oleate on isocitrate lyase activity during the germination of Pinus pinea seeds. Plant Physiol. 1973; 52, 549–553. doi: 10.1104/pp.52.6.549 16658603

62. Hendricks SB, Taylorson RB. Variation in germination and amino acid leakage of seeds with temperature related to membrane phase change. Plant Physiol. 1976; 58, 7–11. doi: 10.1104/pp.58.1.7 16659623

63. Allard RW. Principles of Plant Breeding. John Willey and Sons Inc., New York 1960.


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