Skip to main content
Log in

Melon shoot organization 1, encoding an AGRONAUTE7 protein, plays a crucial role in plant development

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A melon gene MSO1 located on chromosome 10 by map-based cloning strategy, which encodes an ARGONAUTE 7 protein, is responsible for the development of shoot organization.

Abstract

Plant endogenous small RNAs (sRNAs) are involved in various plant developmental processes. In Arabidopsis, sRNAs combined with ARGONAUTE (AGO) proteins are incorporated into the RNA-induced silencing complex (RISC), which functions in RNA silencing or biogenesis of trans-acting siRNAs (ta-siRNAs). However, their roles in melon (Cucumis melo L.) are still unclear. Here, the melon shoot organization 1 (mso1) mutant was identified and shown to exhibit pleiotropic phenotypes in leaf morphology and plant architecture. Positional cloning of MSO1 revealed that it encodes a homologue of Arabidopsis AGO7/ZIPPY, which is required for the production of ta-siRNAs. The AG-to-C mutation in the second exon of MSO1 caused a frameshift mutation and significantly reduced its expression. Ectopic expression of MSO1 rescued the Arabidopsis ago7 phenotype. RNA-seq analysis showed that several genes involved in transcriptional regulation and plant hormones were significantly altered in mso1 compared to WT. A total of 304 and 231 miRNAs were identified in mso1 and WT by sRNA sequencing, respectively, and among them, 42 known and ten novel miRNAs were differentially expressed. cme-miR390a significantly accumulated, and the expression levels of the two ta-siRNAs were almost completely abolished in mso1. Correspondingly, their targets, the ARF3 and ARF4 genes, showed dramatically upregulated expression, indicating that the miR390-TAS3-ARF pathway has conserved roles in melon. These findings will help us better understand the molecular mechanisms of MSO1 in plant development in melon.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

The accession number for MSO1 is OL840913. The complete RNA-seq sequencing and sRNA sequencing data for all the samples were deposited in the NCBI SRA database under accession numbers PRJNA787969 and PRJNA787775, respectively.

References

  • Abe M, Yoshikawa T, Nosaka M, Sakakibara H, Sato Y, Nagato Y, Itoh J (2010) WAVY LEAF1, an ortholog of Arabidopsis HEN1, regulates shoot development by maintaining MicroRNA and trans-acting small interfering RNA accumulation in rice. Plant Physiol 154:1335–1346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouché N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16:927–932

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Khan N, Xie L (2020) Molecular and hormonal regulation of leaf morphogenesis in Arabidopsis. Int J Mol Sci 21:5132

    Article  CAS  PubMed Central  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  CAS  PubMed  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM (2000) Gene ontology: tool for the unification of biology. Gene Ontol Consort Nat Genet 25:25–29

    Article  CAS  Google Scholar 

  • Axtell MJ, Jan C, Rajagopalan R, Bartel DP (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–677

    Article  CAS  PubMed  Google Scholar 

  • Bai S, Tian Y, Tan C, Bai S, Hao J, Hasi A (2020) Genome-wide identification of microRNAs involved in the regulation of fruit ripening and climacteric stages in melon (Cucumis melo). Hortic Res 7:106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Candela H, Johnston R, Gerhold A, Foster T, Hake S (2008) The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves. Plant Cell 20:2073–2087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Deng P, Muhammad S, Cao M, Wu L (2018) Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol J 16:965–975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas RN, Wiley D, Sarkar A, Springefr N, Timmermans MC, Scanlon MJ (2010) Ragged seedling2 encodes an ARGONAUTE7-like protein required for mediolateral expansion, but not dorsiventrality, of maize leaves. Plant Cell 22:1441–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du F, Guan C, Jiao Y (2018) Molecular mechanisms of leaf morphogenesis. Mol Plant 11:1117–1134

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944

    Article  CAS  PubMed  Google Scholar 

  • Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS (2005) Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol 15:331–341

    Article  CAS  PubMed  Google Scholar 

  • Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865

    Article  CAS  PubMed  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 

  • Hunter C, Willmann MR, Wu G, Yoshikawa M, de la Luz G-N, Poethig SR (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133:2973–2981

    Article  CAS  PubMed  Google Scholar 

  • Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nature Reviews Mol Cell Biol 9:22–32

    Article  CAS  Google Scholar 

  • Itoh JI, Kitano H, Matsuoka M, Nagato Y (2000) Shoot organization genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell 12:2161–2174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh J, Sato Y, Nagato Y (2008) The SHOOT ORGANIZATION2 gene coordinates leaf domain development along the central-marginal axis in rice. Plant Cell Physiol 49:1226–1236

    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 

  • Jin S, Zhan J, Zhou Y (2021) Argonaute proteins: structures and their endonuclease activity. Mol Biol Rep 48:4837–4849

    Article  CAS  PubMed  Google Scholar 

  • Lee ZH, Hirakawa T, Yamaguchi N, Ito T (2019) The Roles of plant hormones and their interactions with regulatory genes in determining meristem activity. Int J Mol Sci 20:4065

    Article  CAS  PubMed Central  Google Scholar 

  • Liu S, Gao P, Zhu Q, Zhu Z, Liu H, Wang X, Weng Y, Gao M, Luan F (2020) Resequencing of 297 melon accessions reveals the genomic history of improvement and loci related to fruit traits in melon. Plant Biotechnol J 18:2545–2558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Yang X, Guo M, Lan T, Yu Y, Mo B, Chen X, Gao L, Liu L (2022) TRANS-ACTING SIRNA3-derived short interfering RNAs confer cleavage of mRNAs in rice. Plant Physiol 188:347–362

    Article  CAS  Google Scholar 

  • Ma J, Lei C, Xu X, Hao K, Wang J, Cheng Z, Ma X, Ma J, Zhou K, Zhang X, Guo X, Wu F, Lin Q, Wang C, Zhai H, Wang H, Wan J (2015) Pi64, encoding a novel CC-NBS-LRR protein, confers resistance to leaf and neck blast in rice. Mol Plant Microbe Interact 28:558–568

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Li C, Zong M, Qiu Y, Liu Y, Huang Y, Xie Y, Zhang H, Wang J (2022) CmFSI8/CmOFP13 gene encoding an OVATE family protein controls fruit shape in melon. J Exp Bot 73:1370–1384

    Article  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG orthology (KO) as a controlled vocabulary. Bioinform 21:3787–3793

    Article  CAS  Google Scholar 

  • Matsui A, Mizunashi K, Tanaka M, Kaminuma E, Nguyen AH, Nakajima M, Kim JM, Nguyen DV, Toyoda T, Seki M (2014) tasiRNA-ARF pathway moderates floral architecture in Arabidopsis plants subjected to drought stress. Biomed Res Int 2014:303451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    Article  CAS  PubMed  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141

    Article  CAS  PubMed  Google Scholar 

  • Nagasaki H, Itoh J, Hayashi K, Hibara K, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104:14867–14871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21:750–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roussin-Léveillée C, Silva-Martins G, Moffett P (2020) ARGONAUTE5 represses age-dependent induction of flowering through physical and functional interaction with miR156 in Arabidopsis. Plant Cell Physiol 61:957–966

    Article  PubMed  CAS  Google Scholar 

  • Satoh N, Hong SK, Nishimura A, Matsuoka M, Kitano H, Nagato Y (1999) Initiation of shoot apical meristem in rice: characterization of four SHOOTLESS genes. Development 126:3629–3636

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Shi Z, Wang J, Wan X, Shen G, Wang X, Zhang J (2007) Over-expression of rice OsAGO7 gene induces upward curling of the leaf blade that enhanced erect-leaf habit. Planta 226:99–108

    Article  CAS  PubMed  Google Scholar 

  • Singh RK, Pandey SP (2015) Evolution of structural and functional diversification among plant Argonautes. Plant Signal Behav 10:e1069455

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13:350–358

    Article  CAS  PubMed  Google Scholar 

  • Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Smith SM, Li J (2018) Genetic Regulation of shoot architecture. Annu Rev Plant Biol 69:437–468

    Article  CAS  PubMed  Google Scholar 

  • Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102:9703–9708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Yang J, Cho WC, Zheng Y (2020) Argonaute proteins: structural features, functions and emerging roles. J Adv Res 24:317–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia R, Xu J, Meyers BC (2017) The emergence, evolution, and diversification of the miR390-TAS3-ARF Pathway in land plants. Plant Cell 29:1232–1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:12984–12989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Yang L, Huang H (2007) Transcriptional, post-transcriptional and post-translational regulations of gene expression during leaf polarity formation. Cell Res 17:512–519

    Article  CAS  PubMed  Google Scholar 

  • Xu M, Hu T, Zhao J, Park MY, Earley KW, Wu G, Yang L, Poethig RS (2016) Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in Arabidopsis thaliana. PLoS Genet 12:e1006263

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xue Z, Liu L, Zhang C (2020) Regulation of shoot apical meristem and axillary meristem development in plants. Int J Mol Sci 21:2917

    Article  CAS  PubMed Central  Google Scholar 

  • Yan J, Cai X, Luo J, Sato S, Jiang Q, Yang J, Cao X, Hu X, Tabata S, Gresshoff PM, Luo D (2010) The REDUCED LEAFLET genes encode key components of the trans-acting small interfering RNA pathway and regulate compound leaf and flower development in lotus japonicus. Plant Physiol 152:797–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yano R, Nonaka S, Ezura H (2018) Melonet-DB, a grand RNA-seq gene expression atlas in melon (Cucumis melo L.). Plant Cell Physiol 59:e4

    Article  PubMed  CAS  Google Scholar 

  • Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A, Sabban M, Wachsman G, Alvarez JP, Amsellem Z, Eshed Y (2012) Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24:3575–3589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Z, Luo D, Li G, Yao X, Wang H, Zeng M, Huang H, Cui X (2010) Characterization of the AE7 gene in Arabidopsis suggests that normal cell proliferation is essential for leaf polarity establishment. Plant J 64:331–342

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, Patel DJ, Chua NH (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis argonaute1 cleavage activity to counter plant defense. Genes Dev 20:3255–3268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, Raikhel N, Jin H (2011) Arabidopsis argonaute 2 regulates innate immunity via miRNA393(∗)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42:356–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xia R, Meyers BC, Walbot V (2015) Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr Opin Plant Biol 27:84–90

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Runions A, Mentink RA, Kierzkowski D, Karady M, Hashemi B, Huijser P, Strauss S, Gan X, Ljung K, Tsiantis M (2020) A WOX/Auxin biosynthesis module controls growth to shape leaf form. Curr Biol 30:4857-4868.e6

    Article  CAS  PubMed  Google Scholar 

  • Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092

    Article  CAS  PubMed  Google Scholar 

  • Zhao G, Lian Q, Zhang Z et al (2019) A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet 51:1607–1615

    Article  CAS  PubMed  Google Scholar 

  • Zheng X, Zhu J, Kapoor A, Zhu JK (2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26:1691–1701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong J, He W, Peng Z, Zhang H, Li F, Yao J (2020) A putative AGO protein, OsAGO17, positively regulates grain size and grain weight through OsmiR397b in rice. Plant Biotechnol J 18:916–928

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Han L, Fu C, Wen J, Cheng X, Nakashima J, Ma J, Tang Y, Tan Y, Tadege M, Mysore KS, Xia G, Wang ZY (2013) The trans-acting short interfering RNA3 pathway and no apical meristem antagonistically regulate leaf margin development and lateral organ separation, as revealed by analysis of an argonaute7/lobed leaflet1 mutant in Medicago truncatula. Plant Cell 25:4845–4862

    Article  CAS  PubMed  PubMed Central  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 145:242–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by grants from the Innovation and Development Program of Beijing Vegetable Research Center (KYCX202001-11), the National Natural Science Foundation of China (U21A20229 and 31701937), Construction Program of Science and Technology Innovation Capacity of Beijing Academy of Agriculture and Forestry Sciences (KJCX20200113), Huaibei major science and technology projects (Z2020011), and the Anhui Key Research and Development Project (202104a06020024).

Author information

Authors and Affiliations

Authors

Contributions

JM and CCL co-wrote the manuscript. JM and HJZ conceived this research project and designed the experiments. PG provided help and advice. JSW screened mutants and managed plant growth. YHQ analyzed the RNA-seq and sRNAs data. MZ cloned the MSO1 gene and performed qRT-PCR experiments. All authors have read and approved the manuscript.

Corresponding authors

Correspondence to Jian Ma or Huijun Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Yiqun Weng and Amnon Levi.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1655 kb)

Supplementary file2 (XLS 2770 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, J., Li, C., Gao, P. et al. Melon shoot organization 1, encoding an AGRONAUTE7 protein, plays a crucial role in plant development. Theor Appl Genet 135, 2875–2890 (2022). https://doi.org/10.1007/s00122-022-04156-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-022-04156-2

Navigation