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Identification of small secreted peptides (SSPs) in maize and expression analysis of partial SSP genes in reproductive tissues

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Abstract

Main conclusion

Maize 1,491 small secreted peptides were identified, which were classified according to the character of peptide sequences. Partial SSP gene expressions in reproductive tissues were determined by qRT-PCR.

Small secreted peptides (SSPs) are important cell–cell communication messengers in plants. Most information on plant SSPs come from Arabidopsis thaliana and Oryza sativa, while little is known about the SSPs of other grass species such as maize (Zea mays). In this study, we identified 1,491 SSP genes from maize genomic sequences. These putative SSP genes were distributed throughout the ten maize chromosomes. Among them, 611 SSPs were classified into 198 superfamilies according to their conserved domains, and 725 SSPs with four or more cysteines at their C-termini shared similar cysteine arrangements with their counterparts in other plant species. Moreover, the SSPs requiring post-translational modification, as well as defensin-like (DEFL) proteins, were identified. Further, the expression levels of 110 SSP genes were analyzed in reproductive tissues, including male flower, pollen, silk, and ovary. Most of the genes encoding basal-layer antifungal peptide-like, small coat proteins-like, thioredoxin-like proteins, γ-thionins-like, and DEFL proteins showed high expression levels in the ovary and male flower compared with their levels in silk and mature pollen. The rapid alkalinization factor-like genes were highly expressed only in the mature ovary and mature pollen, and pollen Ole e 1-like genes showed low expression in silk. The results of this study provide basic information for further analysis of SSP functions in the reproductive process of maize.

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Abbreviations

AAI-LTSS:

Alpha amylase inhibitor-lipid transfer and seed storage proteins domain

BAP:

Basal layer antifungal peptide

BBI:

Bowman–Birk type proteinase inhibitor

CEP:

C-terminally encoded peptide

CLE:

CLAVATA3/ESR-related peptide

CLEL:

CLE-like

CLV:

CLAVATA

CRP:

Cysteine-rich peptide

Cu bind-like:

Copper-binding protein-like protein

DEFLs:

Defensin-like protein

Dirigent:

Dirigent-like protein

DPBB:

Double psi beta-barrel structure

EPF:

Epidermal patterning factor

GASA:

Gibberellin regulated cysteine rich protein

GLV:

GOLVEN

GO:

Gene ontology analysis

HDEL:

His-Asp-Glu-Leu sequence

HypSys:

Hydroxyproline-rich systemin

IDA:

Inflorescence deficient in abscission

KDEL:

Lys-Asp-Glu-Leu sequence

LRRNT:

Leucine rich repeat N-terminal domain

ORF:

Open reading frame

PEP:

Plant elicitor peptide

PMEI:

Pectin methylesterase inhibitor

PNP:

Plant natriuretic peptide

Pollen Ole e 1:

Pollen proteins Ole e 1-like protein

PSK:

Phytosulfokine

PSY:

Peptide containing sulfated tyrosine

qRT-PCR:

Quantitative real-time PCR

RALF:

Rapid alkalinization factor

RGF:

Root meristem growth factor

SEA:

Singular enrichment analysis

SCP:

Small coat protein

SCR:

S-locus cysteine-rich protein

SP11:

S-locus protein 11

SSP:

Small secreted peptide

TDIF:

Tracheary element differentiation inhibitory factor

TPD:

Tapetum determinant

References

  • Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci USA 104:18333–18338

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Andrews SJ, Rothnagel JA (2014) Emerging evidence for functional peptides encoded by short open reading frames. Nat Rev Genet 15:193–204

    Article  PubMed  CAS  Google Scholar 

  • Bartels S, Lori M, Mbengue M, van Verk M, Klauser D, Hander T, Böni R, Robatzek S, Boller T (2013) The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J Exp Bot 64:5309–5321

    Article  PubMed  CAS  Google Scholar 

  • Betsuyaku S, Sawa S, Yamada M (2011) The function of the CLE peptides in plant development and plant–microbe interactions. Arabidopsis Book 9:e0149

    Article  PubMed  PubMed Central  Google Scholar 

  • Broekaert WF, Cammue BPA, De Bolle MFC, Thevissen K, De Samblanx GW, Osborn RW (1997) Antimicrobial peptides from plants. Crit Rev Plant Sci 16:297–323

    Article  CAS  Google Scholar 

  • Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB (2003) INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–2307

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen YC, Siems WF, Pearce G, Ryan CA (2008) Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J Biol Chem 283:11469–11476

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Covey PA, Subbaiah CC, Parsons RL, Pearce G, Lay FT, Anderson MA, Ryan CA, Bedinger PA (2010) A pollen-specific RALF from tomato that regulates pollen tube elongation. Plant Physiol 153:703–715

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Czyzewicz N, Yue K, Beeckman T, De Smet I (2013) Message in a bottle: small signalling peptide outputs during growth and development. J Exp Bot 64:5281–5296

    Article  PubMed  CAS  Google Scholar 

  • De Coninck B, Carron D, Tavormina P, Willem L, Craik DJ, Vos C, Thevissen K, Mathys J, Cammue BP (2013) Mining the genome of Arabidopsis thaliana as a basis for the identification of novel bioactive peptides involved in oxidative stress tolerance. J Exp Bot 64:5297–5307

    Article  PubMed  Google Scholar 

  • De Smet I, Voss U, Jürgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173

    Article  PubMed  Google Scholar 

  • Delay C, Imin N, Djordjevic MA (2013) CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. J Exp Bot 64:5383–5394

    Article  PubMed  CAS  Google Scholar 

  • Downs GS, Bi YM, Colasanti J, Wu W, Chen X, Zhu T, Rothstein SJ, Lukens LN (2013) A developmental transcriptional network for maize defines coexpression modules. Plant Physiol 161:1830–1843

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38(Web Server issue):W64–W70

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Endo S, Shinohara H, Matsubayashi Y, Fukuda H (2013) A novel pollen–pistil interaction conferring high-temperature tolerance during reproduction via CLE45 signaling. Curr Biol 23:1670–1676

    Article  PubMed  CAS  Google Scholar 

  • Farrokhi N, Whitelegge JP, Brusslan JA (2008) Plant peptides and peptidomics. Plant Biotechnol J 6:105–134

    Article  PubMed  CAS  Google Scholar 

  • Fernandez A, Drozdzecki A, Hoogewijs K, Nguyen A, Beeckman T, Madder A, Hilson P (2013a) Transcriptional and functional classification of the GOLVEN/ROOT GROWTH FACTOR/CLE-like signaling peptides reveals their role in lateral root and hair formation. Plant Physiol 161:954–970

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fernandez A, Hilson P, Beeckman T (2013b) GOLVEN peptides as important regulatory signalling molecules of plant development. J Exp Bot 64:5263–5268

    Article  PubMed  CAS  Google Scholar 

  • Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914

    Article  PubMed  CAS  Google Scholar 

  • Gambino G, Perrone I, Gribaudo I (2008) A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 19:520–525

    Article  PubMed  CAS  Google Scholar 

  • Hanada K, Zhang X, Borevitz JO, Li WH, Shiu SH (2007) A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res 17:632–640

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hayama R, Izawa T, Shimamoto K (2002) Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. Plant Cell Physiol 43:494–504

    Article  PubMed  CAS  Google Scholar 

  • Higashiyama T (2010) Peptide signaling in pollen–pistil interactions. Plant Cell Physiol 51:177–189

    Article  PubMed  CAS  Google Scholar 

  • Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA 105:15208–15213

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang Y, Tao Z, Liu Q, Wang X, Yu J, Liu G, Wang H (2014) BnEPFL6, an EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) secreted peptide gene, is required for filament elongation in Brassica napus. Plant Mol Biol. doi:10.1007/s11103-014-0200-2

    Google Scholar 

  • Hueros G, Varotto S, Salamini F, Thompson RD (1995) Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7:747–757

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098–10103

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol 155:1325–1338

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–845

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Borevitz JO, Preuss D (2007) Genome-wide expression profiling of the Arabidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genet 3:1848–1861

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100:16125–16130

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  PubMed  CAS  Google Scholar 

  • Lakhssassi N, Doblas VG, Rosado A, del Valle AE, Posé D, Jimenez AJ, Castillo AG, Valpuesta V, Borsani O, Botella MA (2012) The Arabidopsis TETRATRICOPEPTIDE THIOREDOXIN-LIKE gene family is required for osmotic stress tolerance and male sporogenesis. Plant Physiol 158:1252–1266

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lauzurica P, Gurbindo C, Maruri N, Galocha B, Diaz R, Gonzalez J, García R, Lahoz C (1988) Olive (olea europea) pollen allergens-I. Immunochemical characterization by immunoblotting, CRIE and immunodetection by a monoclonal antibody. Mol Immunol 25:329–335

    Article  PubMed  CAS  Google Scholar 

  • Lease KA, Walker JC (2006) The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol 142:831–838

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ludidi NN, Heazlewood JL, Seoighe C, Irving HR, Gehring CA (2002) Expansin-like molecules: novel functions derived from common domains. J Mol Evol 54:587–594

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39(Database issue):D225–D229

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell–cell communication in plant reproduction and development. J Exp Bot 62:1677–1686

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi Y (2011a) Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol 52:5–13

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Matsubayashi Y (2011b) Small post-translationally modified peptide signals in Arabidopsis. Arabidopsis Book 9:e0150

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsubayashi Y (2014) Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol 65:385–413

    Article  PubMed  Google Scholar 

  • Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y (2006) Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol 142:45–53

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–1067

    Article  PubMed  CAS  Google Scholar 

  • Meng L, Buchanan BB, Feldman LJ, Luan S (2012) CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc Natl Acad Sci USA 109:1760–1765

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Miwa H, Tamaki T, Fukuda H, Sawa S (2009) Evolution of CLE signaling: origins of the CLV1 and SOL2/CRN receptor diversity. Plant Signal Behav 4:477–481

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Murphy E, Smith S, De Smet I (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198–3217

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Napier RM, Fowke LC, Hawes C, Lewis M, Pelham HR (1992) Immunological evidence that plants use both HDEL and KDEL for targeting proteins to the endoplasmic reticulum. J Cell Sci 102(Pt 2):261–271

    PubMed  CAS  Google Scholar 

  • Ohyama K, Shinohara H, Ogawa-ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580

    Article  PubMed  CAS  Google Scholar 

  • Ohyama K, Ogawa M, Matsubayashi Y (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC–MS-based structure analysis. Plant J 55:152–160

    Article  PubMed  CAS  Google Scholar 

  • Pan B, Sheng J, Sun W, Zhao Y, Hao P, Li X (2013) OrysPSSP: a comparative platform for small secreted peptides from rice and other plants. Nucleic Acids Res 41(Database issue):D1192–D1198

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pearce G, Ryan CA (2003) Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J Biol Chem 278:30044–30050

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Moura DS, Stratmann J, Ryan CA Jr (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 98:12843–12847

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pearce G, Siems WF, Bhattacharya R, Chen YC, Ryan C (2007) Three hydroxyproline-rich glycopeptides derived from a single petunia polyprotein precursor activate defensin I, a pathogen defense response gene. J Biol Chem 282:17777–17784

    Article  PubMed  CAS  Google Scholar 

  • Pelegrini PB, Franco OL (2005) Plant γ-thionins: novel insights on the mechanism of action of a multi-functional class of defense proteins. Int J Biochem Cell Biol 37:2239–2253

    Article  PubMed  CAS  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  PubMed  CAS  Google Scholar 

  • Rholam M, Fahy C (2009) Processing of peptide and hormone precursors at the dibasic cleavage sites. Cell Mol Life Sci 66:2075–2791

    Article  PubMed  CAS  Google Scholar 

  • Roberts I, Smith S, De Rybel B, Van Den Broeke J, Smet W, De Cokere S, Mispelaere M, De Smet I, Beeckman T (2013) The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. J Exp Bot 64:5371–5381

    Article  PubMed  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  PubMed  CAS  Google Scholar 

  • Serna A, Maitz M, O’Connell T, Santandrea G, Thevissen K, Tienens K, Hueros G, Faleri C, Cai G, Lottspeich F, Thompson RD (2001) Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J 25:687–698

    Article  PubMed  CAS  Google Scholar 

  • Silverstein KA, Graham MA, Paape TD, VandenBosch KA (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Silverstein KA, Moskal WA Jr, Wu HC, Underwood BA, Graham MA, Town CD, VandenBosch KA (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51:262–280

    Article  PubMed  CAS  Google Scholar 

  • Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–244

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi H, Higashiyama T (2012) A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol 10:e1001449

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Van der Weerden NL, Anderson MA (2013) Plant defensins: common fold, multiple functions. Fungal Biol Rev 26:121–131

    Article  Google Scholar 

  • Wang YH, Gehring C, Irving HR (2011) Plant natriuretic peptides are apoplastic and paracrine stress response molecules. Plant Cell Physiol 52:837–850

    Article  PubMed  CAS  Google Scholar 

  • Wheeler JI, Irving HR (2012) Plant peptide signaling: an evolutionary adaptation. In: Irving HR, Gehring C (eds) Plant signaling peptides. Springer, Berlin, pp 1–23

    Chapter  Google Scholar 

  • Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105:18625–18630

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Whitford R, Fernandez A, Tejos R, Pérez AC, Kleine-Vehn J, Vanneste S, Drozdzecki A, Leitner J, Abas L, Aerts M, Hoogewijs K, Baster P, De Groodt R, Lin YC, Storme V, Van de Peer Y, Beeckman T, Madder A, Devreese B, Luschnig C, Friml J, Hilson P (2012) GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev Cell 22:678–685

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (1999) Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants. Proc Natl Acad Sci USA 96:13560–13565

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) TAPETUM DETERMINANT 1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yang X, Tschaplinski TJ, Hurst GB, Jawdy S, Abraham PE, Lankford PK, Adams RM, Shah MB, Hettich RL, Lindquist E, Kalluri UC, Gunter LE, Pennacchio C, Tuskan GA (2011) Discovery and annotation of small proteins using genomics, proteomics, and computational approaches. Genome Res 21:634–641

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This study is funded by the Major Research Plan from the Ministry of Science and Technology of China (No. 2013CB945100) and the National Natural Science Foundation of China (No. 31170293 and No. 31270358).

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  1. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, 271018, Shandong, China

    Ye Long Li, Xin Ren Dai, Xin-Qi Gao & Xian Sheng Zhang

  2. College of Information Sciences and Engineering, Shandong Agricultural University, Taian, Shandong, China

    Xun Yue

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  1. Ye Long Li
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Correspondence to Xin-Qi Gao.

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Y. L. Li and X. R. Dai have contribute equally to this work.

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Li, Y.L., Dai, X.R., Yue, X. et al. Identification of small secreted peptides (SSPs) in maize and expression analysis of partial SSP genes in reproductive tissues. Planta 240, 713–728 (2014). https://doi.org/10.1007/s00425-014-2123-1

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