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A tripartite approach identifies the major sunflower seed albumins

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Abstract

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We have used a combination of genomic, transcriptomic, and proteomic approaches to identify the napin-type albumin genes in sunflower and define their contributions to the seed albumin pool.

Abstract

Seed protein content is determined by the expression of what are typically large gene families. A major class of seed storage proteins is the napin-type, water soluble albumins. In this work we provide a comprehensive analysis of the napin-type albumin content of the common sunflower (Helianthus annuus) by analyzing a draft genome, a transcriptome and performing a proteomic analysis of the seed albumin fraction. We show that although sunflower contains at least 26 genes for napin-type albumins, only 15 of these are present at the mRNA level. We found protein evidence for 11 of these but the albumin content of mature seeds is dominated by the encoded products of just three genes. So despite high genetic redundancy for albumins, only a small sub-set of this gene family contributes to total seed albumin content. The three genes identified as producing the majority of sunflower seed albumin are potential future candidates for manipulation through genetics and breeding.

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References

  • Allen RD, Cohen EA, Vonder Haar RA, Adams CA, Ma DP, Nessler CL, Thomas TL (1987) Sequence and expression of a gene encoding an albumin storage protein in sunflower. Mol Gen Genet 210:211–218

    Article  PubMed  CAS  Google Scholar 

  • Blundy KS, Blundy MAC, Crouch ML (1991) Differential expression of members of the napin storage protein gene family during embryogenesis in Brassica napus. Plant Mol Biol 17:1099–1104

    Article  PubMed  CAS  Google Scholar 

  • Boutilier K, Hattori J, Baum BR, Miki BL (1999) Evolution of 2S albumin seed storage protein genes in the Brassicaceae. Biochem Syst Ecol 27:223–234

    Article  CAS  Google Scholar 

  • Chibani K, Ali-Rachedi S, Job C, Job C, Jullien M, Grappin P (2006) Proteomic analysis of seed dormancy in Arabidopsis. Plant Physiol 142:1493–1510

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Christie M, Croft LJ, Carroll BJ (2011) Intron splicing suppresses RNA silencing in Arabidopsis. Plant J 68:159–167

    Article  PubMed  CAS  Google Scholar 

  • Chu Y et al (2008) Reduction of IgE binding and nonpromotion of Aspergillus flavus fungal growth by simultaneously silencing Ara h 2 and Ara h 6 in peanut. J Agric Food Chem 56:11225–11233

    Article  PubMed  CAS  Google Scholar 

  • Elliott AG et al (2014) Evolutionary origins of a bioactive peptide buried within preproalbumin. Plant Cell 26:981–995

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ericson ML, Rödin J, Lenman M, Glimelius K, Josefsson LG, Rask L (1986) Structure of the rapeseed 1.7 S storage protein, napin, and its precursor. J Biol Chem 261:14576–14581

    PubMed  CAS  Google Scholar 

  • Freire JEC et al (2015) Mo-CBP3, an Antifungal chitin-binding protein from Moringa oleifera seeds, is a member of the 2S albumin family. PLoS One 10:e0119871

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hummel M, Wigger T, Brockmeyer J (2015) Characterization of mustard 2S albumin allergens by bottom-up, middle-down, and top-down proteomics: a consensus set of isoforms of Sin a 1. J Proteome Res 14:1547–1556

    Article  PubMed  CAS  Google Scholar 

  • Irwin SD, Keen JN, Findlay JBC, Lord JM (1990) The Ricinus communis 2S albumin precursor: a single preproprotein may be processed into two different heterodimeric storage proteins. Mol Gen Genet 222:400–408

    Article  PubMed  CAS  Google Scholar 

  • Jayasena AS, Secco D, Bernath-Levin K, Berkowitz O, Whelan J, Mylne JS (2014) Next generation sequencing and de novo transcriptomics to study gene evolution. Plant Methods 10:34

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiang C, Cheng Z, Zhang C, Yu T, Zhong Q, Shen J, Huang X (2014) Proteomic analysis of seed storage proteins in wild rice species of the Oryza genus. Proteome Sci 12:51

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kortt AA, Caldwell JB (1990) Low molecular weight albumins from sunflower seed: identification of a methionine-rich albumin. Phytochemistry 29:2805–2810

    Article  CAS  Google Scholar 

  • Kortt AA, Caldwell JB, Lilley GG, Higgins TJV (1991) Amino acid and cDNA sequences of a methionine-rich 2S protein from sunflower seed (Helianthus annuus L.). Eur J Biochem 195:329–334

    Article  PubMed  CAS  Google Scholar 

  • Krebbers E et al (1988) Determination of the processing sites of an Arabidopsis 2S albumin and characterization of the complete gene family. Plant Physiol 87:859–866

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kreis M, Shewry PR (1989) Unusual features of cereal seed protein structure and evolution. BioEssays 10:201–207

    Article  PubMed  CAS  Google Scholar 

  • Lehmann K et al (2006) Structure and stability of 2S albumin-type peanut allergens: implications for the severity of peanut allergic reactions. Biochem J 395:463–472

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Maria-Neto S et al (2011) Bactericidal activity identified in 2S albumin from sesame seeds and in silico studies of structure–function relations. Protein J 30:340–350

    Article  PubMed  CAS  Google Scholar 

  • Meinke D, Koornneef M (1997) Community standards for Arabidopsis genetics. Plant J 12:247–253

    Article  CAS  Google Scholar 

  • Menéndez-Arias L, Moneo I, DomÍNguez J, RodrÍGuez R (1988) Primary structure of the major allergen of yellow mustard (Sinapis alba L.) seed, Sin a I. Eur J Biochem 177:159–166

    Article  PubMed  Google Scholar 

  • Moreno FJ, Jenkins JA, Mellon FA, Rigby NM, Robertson JA, Wellner N, Clare Mills EN (2004) Mass spectrometry and structural characterization of 2S albumin isoforms from Brazil nuts (Bertholletia excelsa). Biochim Biophys Acta 1698:175–186

    Article  PubMed  CAS  Google Scholar 

  • Moro CF et al (2015) Unraveling the seed endosperm proteome of the lotus (Nelumbo nucifera Gaertn.) utilizing 1DE and 2DE separation in conjunction with tandem mass spectrometry. Proteomics 00:1–19

    Google Scholar 

  • Mylne JS et al (2011) Albumins and their processing machinery are hijacked for cyclic peptides in sunflower. Nat Chem Biol 7:257–259

    Article  PubMed  CAS  Google Scholar 

  • Mylne JS, Hara-Nishimura I, Rosengren KJ (2014) Seed storage albumins: biosynthesis, trafficking and structures. Funct Plant Biol 41:671–677

    Article  CAS  Google Scholar 

  • Nordlee JA, Taylor SL, Townsend JA, Thomas LA, Bush RK (1996) Identification of a Brazil-Nut allergen in transgenic soybeans. N Engl J Med 334:688–692

    Article  PubMed  CAS  Google Scholar 

  • Nott A, Meislin SH, Moore MJ (2003) A quantitative analysis of intron effects on mammalian gene expression. RNA 9:607–617

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rajjou L, Lovigny Y, Groot SPC, Belghazi M, Job C, Job D (2008) Proteome-wide characterization of seed aging in Arabidopsis: a comparison between artificial and natural aging protocols. Plant Physiol 148:620–641

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Raynal M, Depigny D, Grellet F, Delseny M (1991) Characterization and evolution of napin-encoding genes in radish and related crucifers. Gene 99:77–86

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro SFF et al (2012) Antifungal and other biological activities of two 2S albumin-homologous proteins against pathogenic fungi. Protein J 31:59–67

    Article  PubMed  CAS  Google Scholar 

  • Scofield SR, Crouch ML (1987) Nucleotide sequence of a member of the napin storage protein family from Brassica napus. J Biol Chem 262:12202–12208

    PubMed  CAS  Google Scholar 

  • Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958

    Article  PubMed  CAS  Google Scholar 

  • Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7:945–956

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Terras FR et al (1992) Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J Biol Chem 267:15301–15309

    PubMed  CAS  Google Scholar 

  • Thorpe SC, Kemeny DM, Panzani RC, McGurl B, Lord M (1988) Allergy to castor bean: II. Identification of the major allergens in castor bean seeds. J Allergy Clin Immunol 82:67–72

    Article  PubMed  CAS  Google Scholar 

  • Thoyts PJE, Napier JA, Millichip M, Stobart AK, Griffiths WT, Tatham AS, Shewry PR (1996) Characterization of a sunflower seed albumin which associates with oil bodies. Plant Sci 118:119–125

    Article  CAS  Google Scholar 

  • van der Klei H, Damme JV, Casteels P, Krebbers E (1993) A fifth 2S albumin isoform is present in Arabidopsis thaliana. Plant Physiol 101:1415–1416

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang K et al (2010) Characterization of seed proteome in Brachypodium distachyon. J Cereal Sci 52:177–186

    Article  CAS  Google Scholar 

  • Wong P-F, Abubakar S (2005) Post-germination changes in Hevea brasiliensis seeds proteome. Plant Sci 169:303–311

    Article  CAS  Google Scholar 

  • Zhou Y et al (2013) Peanut allergy, allergen composition, and methods of reducing allergenicity: a review. Int J Food Sci Technol 2013:1–8

    Article  CAS  Google Scholar 

Download references

Acknowledgments

A.S.J. is supported by an International Postgraduate Research Scholarship and an Australian Postgraduate Award. B.F. was supported by Australian Research Council grant DP120103369. J.R. and J.S.M. are supported by Australian Research Council Future Fellowships FT130100890 and FT120100013, respectively. Authors would like to acknowledge Prof. Loren Rieseberg (University of British Columbia) for providing access to a draft sunflower genome, the BAC/EST Resource Center of the Arizona Genomics Institute (University of Arizona) and David Kudrna for H. annuus cDNA clones and the Compositae Genome Project website (http://cgpdb.ucdavis.edu/) supported by the USDA IFAFS Programme and NSF Plant Genome Programme for EST data. The authors also thank Michelle Colgrave, Nicolas Taylor, Richard Jacoby and Mark Condina for valuable advice on proteomics. This work was supported by Australian Research Council grant DP130101191.

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Correspondence to Joshua S. Mylne.

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Communicated by B. Hulke.

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122_2015_2653_MOESM1_ESM.txt

Supplementary Data Set 1. FASTA list of all 26 sunflower preproalbumin sequences (SESA1-SESA21, PawL1-PawL3, PawS1 and PawS2). (TXT 4 kb)

122_2015_2653_MOESM2_ESM.eps

Supplementary Fig. 1 Alignment of the predicted sunflower albumin sequences. (A) Alignment of dimeric albumins. (B) Alignment of double albumins. (C) Alignment of PawS-type albumins. Sequences were aligned using CLC Genomics Workbench 7.5.1 setting the alignment parameters specifically as gap open cost: 9, gap extension cost: 2 and rendered using BOXSHADE. Based on similarity sequences were ordered by CLC automatically. Predicted ER signal (ER), small albumin subunit (SSU), large albumin subunit (LSU), PawS-derived peptide (PDP in PawS) or the PDP-like (in PawL) region, and spacer regions are marked in rose, green, orange, aqua, and black, respectively. Region delimitation was inferred by observing the Cys residue pattern and the potential albumin maturation sites. Red boxes indicate the conserved Cys residues. Partial ORFs are indicated by two lines at the distal ends of the sequence. (EPS 3951 kb)

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Jayasena, A.S., Franke, B., Rosengren, J. et al. A tripartite approach identifies the major sunflower seed albumins. Theor Appl Genet 129, 613–629 (2016). https://doi.org/10.1007/s00122-015-2653-3

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