Skip to main content

Advertisement

SpringerLink
Log in

Global identification and expression analysis of stress-responsive genes of the Argonaute family in apple

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Argonaute (AGO) proteins, which are found in yeast, animals, and plants, are the core molecules of the RNA-induced silencing complex. These proteins play important roles in plant growth, development, and responses to biotic stresses. The complete analysis and classification of the AGO gene family have been recently reported in different plants. Nevertheless, systematic analysis and expression profiling of these genes have not been performed in apple (Malus domestica). Approximately 15 AGO genes were identified in the apple genome. The phylogenetic tree, chromosome location, conserved protein motifs, gene structure, and expression of the AGO gene family in apple were analyzed for gene prediction. All AGO genes were phylogenetically clustered into four groups (i.e., AGO1, AGO4, MEL1/AGO5, and ZIPPY/AGO7) with the AGO genes of Arabidopsis. These groups of the AGO gene family were statistically analyzed and compared among 31 plant species. The predicted apple AGO genes are distributed across nine chromosomes at different densities and include three segment duplications. Expression studies indicated that 15 AGO genes exhibit different expression patterns in at least one of the tissues tested. Additionally, analysis of gene expression levels indicated that the genes are mostly involved in responses to NaCl, PEG, heat, and low-temperature stresses. Hence, several candidate AGO genes are involved in different aspects of physiological and developmental processes and may play an important role in abiotic stress responses in apple. To the best of our knowledge, this study is the first to report a comprehensive analysis of the apple AGO gene family. Our results provide useful information to understand the classification and putative functions of these proteins, especially for gene members that may play important roles in abiotic stress responses in M. hupehensis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AGO:

Argonaute

DCL:

Dicer-like

dsRNA:

Double-strands RNA

miRNA:

microRNA

pri-miRNA:

Primary miRNA

RDR:

RNA dependent RNA polymerase

RISC:

RNA-induced silencing complex

siRNA:

Small interfering RNA

sRNA:

Small RNA

ssRMA:

Single-stranded RNA

BLAST:

The Basic Local Alignment Search Tool

GWD:

Genome-Wide Duplication

HMM:

Hidden Markov Model

MEGA:

Molecular Evolutionary Genetics Analysis

MUSCLE:

Multiple Sequence Comparison by Log-Expectation

NJ:

The neighbor-joining

SMART:

A Simple Modular Architecture Research Tool

Apple GFDB database:

Apple Gene Function and Gene Family Database

GDR:

Genome Database for Rosaceae

Pfam:

Protein family

GSDS:

Gene Structure Display Server

ORF:

Open reading frame

MW:

Molecular weight

Aa:

Amino acid

pIs:

Isoelectric points

UTR:

Untranslated region

qRT-PCR:

Quantitative real-time reverse transcription-PCR

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bai M, Yang GS, Chen WT, Mao ZC, Kang HX, Chen GH, Yang YH, Xie BY (2012) Genome-wide identification of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analyses in response to viral infection and abiotic stresses in Solanum lycopersicum. Gene 501:52–62

    Article  CAS  PubMed  Google Scholar 

  • Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Nati Acad Sci USA 102:11928–11933

    Article  CAS  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Schaller H, Khafif M, Schott G, Bendahmane A, Voinnet O (2012) Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis. Proc Nati Acad Sci USA 109:1778–1783

    Article  CAS  Google Scholar 

  • Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA, Nguyen T, Cuperus JT, Carrington JC (2012) Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24:3613–3629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimick PS, Hoskin JC (1983) Review of apple flavor-state of the art. Crit Rev Food Sci Nutr 18:387–409

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  PubMed  PubMed Central  Google Scholar 

  • Faehnle CR, Joshua-Tor L (2007) Argonautes confront new small RNAs. Curr Opin Chem Biol 11:569–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giorno F, Guerriero G, Baric S, Mariani C (2012) Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genom 13:639

    Article  CAS  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  CAS  PubMed  Google Scholar 

  • Harvey JJ, Lewsey MG, Patel K, Westwood J, Heimstädt S, Carr JP, Baulcombe DC (2011) An antiviral defense role of AGO2 in plants. PLoS ONE 6:e14639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hock J, Meister G (2008) The Argonaute protein family. Genome Biol 9:210

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunter C, Sun H, Poethig RS (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739

    Article  CAS  PubMed  Google Scholar 

  • Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 1:22–32

    Article  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  CAS  PubMed  Google Scholar 

  • Ji L, Liu X, Yan J, Wang W, Yumul RE, Kim YJ, Dinh TT, Liu J, Cui X, Zheng B, Agarwal M, Liu C, Cao X, Tang G, Chen X (2011) ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 7:e1001358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapoor M, Arora R, Lama T, Nijhawan A, Khurana JP, Tyagi AK, Kapoor S (2008) Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genom 9:451

    Article  Google Scholar 

  • Kidner CA, Martienssen RA (2005) The role of ARGONAUTE1 (AGO1) in meristem formation and identity. Dev Biol 280:504–517

    Article  CAS  PubMed  Google Scholar 

  • Kim NV (2008) Sorting out small RNA. Cell 133:25–26

    Article  CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SY, Chang SS, Shin JH, Kang DH (2007) Membrane filtration method for enumeration and isolation of Alicyclobacillus spp. from apple juice. Lett Appl Microbiol 45:540–546

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305

    Article  CAS  PubMed  Google Scholar 

  • Li YZ, Wu BJ, Yu YL, Yang GD, Wu CA, Zheng CC (2011) Genome-wide analysis of the RING finger gene family in apple. Mol Genet Genomics 286:81–94

    Article  CAS  PubMed  Google Scholar 

  • Li J, Hou HM, Li XQ, Xiang J, Yin XJ, Gao H, Zheng Y, Bassett CL, Wang XP (2013a) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus × domestica Borkh.). Plant Physiol Bioch 70:100–114

    Article  CAS  Google Scholar 

  • Li XQ, Guo RR, Li J, Singer SD, Zhang YC, Yin XJ, Zheng Y, Fan CH, Wang XP (2013b) Genome-wide identification and analysis of the aldehyde dehydrogenase (ALDH) gene superfamily in apple (Malus × domestica Borkh.). Plant Physiol Bioch 71:268–282

    Article  CAS  Google Scholar 

  • Liang D, Xia H, Wu S, Ma F (2012) Genome-wide identification and expression profiling of dehydrin gene family in Malus domestica. Mol Biol Rep 39:10759–10768

    Article  CAS  PubMed  Google Scholar 

  • Luo XC, Sun MH, Xu RR, Shu HR, Wang JW, Zhang SZ (2014) Genomewide identification and expression analysis of the ARF gene family in apple. J Genet 93:785–797

    Article  PubMed  Google Scholar 

  • Mallory A, Vaucheret H (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:3879–3889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manavella PA, Weigel D, Wu L (2011) Argonaute10 as a miRNA locker. Cell 145:173–174

    Article  CAS  PubMed  Google Scholar 

  • Mistry J, Finn R (2007) Pfam: a domain-centric method for analyzing proteins and proteomes. Methods Mol Biol 396:43–58

    Article  CAS  PubMed  Google Scholar 

  • Montgomery TA, Yoo SJ, Fahlgren N, Gilbert SD, Howell MD, Sullivan CM, Alexander A, Nguyen G, Allen E, Ahn JH, Carrington JC (2008) Inaugural article: AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Nati Acad Sci USA 105:20055–20062

    Article  CAS  Google Scholar 

  • Newman KL, Fernandez AG, Barton MK (2002) Regulation of Axis Determinacy by the Arabidopsis PINHEAD Gene. Plant Cell 14:3029–3042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M (2002) OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J 30:189–201

    Article  CAS  PubMed  Google Scholar 

  • Palmer LE, Rabinowicz PD, O’Shaughnessy AL, Balija VS, Nascimento LU, Dike S, de la Bastide M, Martienssen RA, McCombie WR (2003) Maize genome sequencing by methylation filtration. Science 302:2115–2117

    Article  PubMed  Google Scholar 

  • Paszkowski J, Rowley MJ, Avrutsky MI, Sifuentes CJ, Pereira L, Wierzbicki AT (2011) Independent chromatin binding of ARGONAUTE4 and SPT5L/KTF1 mediates transcriptional gene silencing. PLoS Genet 7:e1002120

    Article  Google Scholar 

  • Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X, Ma Q, Zhu S, Cheng B (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS ONE 7:e40120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen C, Vaucheret H, Brodersen P (2013) Lessons on RNA silencing mechanisms in plants from Eukaryotic Argonaute structures. Plant Cell 25:22–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian Y, Cheng Y, Cheng X, Jiang H, Zhu S, Cheng B (2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep 30:1347–1363

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506

    Article  CAS  PubMed  Google Scholar 

  • Shao FJ, Lu SF (2013) Genome-wide identification, molecular cloning, expression profiling and posttranscriptional regulation analysis of the Argonaute gene family in Salvia miltiorrhiza, an emerging model medicinal plant. BMC Genom 14:512

    Article  CAS  Google Scholar 

  • Song JJ, Joshua-Tor L (2006) Argonaute and RNA-getting into the groove. Curr Opin Struct Biol 16:5–11

    Article  CAS  PubMed  Google Scholar 

  • Su HY, Zhang SZ, Yuan XW, Chen CT, Wang XF, Hao YJ (2013) Genome-wide analysis and identification of stress-responsive genes of the NAM–ATAF1, 2–CUC2 transcription factor family in apple. Plant Physiol Biochem 71:11–21

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • The Arabidopsis Genome Iniative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Tian Y, Dong QL, Ji ZR, Chi FM, Cong PH, Zhou ZS (2015) Genome-wide identification and analysis of the MADS-box gene family in apple. Gene 555:277–290

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H, Vazquez F, Crété P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Juranek S, Li H, Sheng G, Tuschl T, Patel DJ (2008) Structure of an Argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456:921–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XB, Jovel J, Udomporn P, Wang Y, Wu Q, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011) The 21-Nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23:1625–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XF, Zhang SZ, Su L, Liu X, Hao YJ (2013) A genome-wide analysis of the LBD (LATERAL ORGAN BOUNDARIES Domain) gene family in Malus domestica with a functional characterization of MdLBD11. PLoS One 8:e57044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitelaw CA, Barbazuk WB, Pertea G, Chan AP, Cheung F, Lee Y, Zheng L, van Heeringen S, Karamycheva S, Bennetzen JL, SanMiguel P, Lakey N, Bedell J, Yuan Y, Budiman MA, Resnick A, Van Aken S, Utterback T, Riedmuller S, Williams M, Feldblyum T, Schubert K, Beachy R, Fraser CM, Quackenbush J (2003) Enrichment of gene-coding sequences in maize by genome filtration. Science 302:2118–2220

    Article  PubMed  Google Scholar 

  • Wu X, Song C, Wang B, Cheng J (2002) Hidden Markov model used in protein sequence analysis. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 19:455–458

    CAS  PubMed  Google Scholar 

  • Xu RR, Sun P, Jia FJ, Lu LT, Li YY, Zhang SZ, Huang JG (2014) Genomewide analysis of TCP transcription factor gene family in Malus domestica. J Genet 93:733–746

    Article  CAS  PubMed  Google Scholar 

  • Ye R, Wang W, Iki T, Liu C, Wu Y, Ishikawa M, Zhou X, Qi Y (2012) Cytoplasmic assembly and selective nuclear import of Arabidopsis ARGONAUTE4/siRNA complexes. Mol Cell 46:859–870

    Article  CAS  PubMed  Google Scholar 

  • Yuan HZ, Zhao K, Lei HJ, Shen XJ, Liao X, Li TH (2013) Genome-wide analysis of the GH3 family in apple (Malus × domestica). BMC Genom 14:297

    Article  CAS  Google Scholar 

  • Zhang SZ, Xu RR, Luo XC, Jiang ZS, Shu HR (2013) Genome-wide identification and expression analysis of MAPK and MAPKK gene family in Malus domestica. Gene 531:377–387

    Article  CAS  PubMed  Google Scholar 

  • Zhang SZ, Xu RR, Gao Z, Chen CT, Jiang ZS, Shu HR (2014) A genome-wide analysis of the expansin genes in Malus × Domestica. Mol Genet Genomics 289:225–236

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Liang D, Wang P, Liu J, Ma F (2012) Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol Genet Genomics 287:423–436

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 2:242–256

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by the National Natural Science Foundation (Grant No. 31401822), the National Natural Science Foundation (Grant No. 31400225), and the Shandong Province Young and Middle-aged Scientists Research Awards Fund (Grant No. BS2014SW014) in China.

Author information

Authors and Affiliations

  1. Key Laboratory of Biology and Molecular Biology in University of Shandong, Weifang University, Weifang, Shandong, 261061, China

    Ruirui Xu & Caiyun Liu

  2. State Key Laboratory of Crop Biology, National Research Center for Apple Engineering and Technology, College of Horticulture Science and Technology, Shandong Agricultural University, 61# Daizong Street, Tai’an, Shandong, 271018, China

    Ning Li & Shizhong Zhang

Authors
  1. Ruirui Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caiyun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ning Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shizhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ruirui Xu or Shizhong Zhang.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, R., Liu, C., Li, N. et al. Global identification and expression analysis of stress-responsive genes of the Argonaute family in apple. Mol Genet Genomics 291, 2015–2030 (2016). https://doi.org/10.1007/s00438-016-1236-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-016-1236-6

Keywords

Search

Navigation