Skip to main content
SpringerLink
Log in

Plasmodesmata play a critical role in promoting the germination of floral buds in Ilex verticillata

  • Brief communication
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

In the plant, plasmodesmata (PDs) permit direct cytoplasmic connections and facilitate the local molecular exchange of neighboring cells. Cell-to-cell communications through PD play critical roles in the small RNAs mobile, transport of metabolites, cell fate specification and development. The trafficking of PD is under tight control and it is also constantly fine-tuned to fit in the requirements of cell-to-cell communication. However, how PD involved in the transition from the dormant to the germination of buds is not yet clearly known. Here, we provide experimental evidence that PD formation and permeability are correlated to the germination of buds in North-American holly. Moreover, the increased PD number and permeability in the germinating buds are associated with the down-regulated SA signaling, which also facilitates starch degradation. Altogether, our study stresses the fundamental role of PD in governing the transition from dormant to germination of floral buds, unveiling the regulation of PD during the flowering of North-American holly. Understanding the mechanism of SA-mediated PD regulation during the flowering will provide an effective way to enhance the improvement of agronomical tree traits by the application of PD engineering.

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

References

  • Amsbury S, Kirk P, Benitez-Alfonso Y (2017) Emerging models on the regulation of intercellular transport by plasmodesmata-associated callose. J Exp Bot 69(1):105–115

    Article  CAS  Google Scholar 

  • Anisimov AV, Egorov AG (2002) Plasmodesmata as a modulator of osmotic water fluxes in plants. Russ J Plant Physiol 49:677–684

    Article  CAS  Google Scholar 

  • Bahaji A, Li J, Sánchez-López Á et al (2014) Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnol Adv 32:87–106

    Article  CAS  Google Scholar 

  • Birren BW, Nusbaum C, Lindblad-Toh K et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  Google Scholar 

  • Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using diamond. Nat Methods 12(1):59–60

    Article  CAS  Google Scholar 

  • Burch-Smith TM, Stonebloom S, Xu M et al (2011) Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248:61–74

    Article  CAS  Google Scholar 

  • Cilia ML, Jackson D (2004) Plasmodesmata form and function. Curr Opin Cell Biol 16:500–506

    Article  CAS  Google Scholar 

  • Clare S, Carole T, Kim F et al (2009) An arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21:581–594

    Article  Google Scholar 

  • Daum G, Medzihradszky A, Suzaki T et al (2014) A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. P Natl Acad Sci USA 111:14619–14624

    Article  CAS  Google Scholar 

  • Faulkner C, Petutschnig E, Benitez-Alfonso Y et al (2013) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci USA 110:9166–9170

    Article  CAS  Google Scholar 

  • Faulkner C (2018) Plasmodesmata and the symplast. Curr Biol 28:R1374–R1378

    Article  CAS  Google Scholar 

  • Fitzgibbon J, Bell K, King E et al (2010) Super-resolution imaging of plasmodesmata using three-dimensional structured illumination microscopy. Plant Physiol 153:1453–1463

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  CAS  Google Scholar 

  • He Y, Zhou KY, Wu ZM et al (2019) Highly efficient nanoscale snalysis of plant dtomata and cell surface using polyaddition silicone rubber. Front Plant Sci 10:1569

    Article  Google Scholar 

  • Hong J, Jiang DA, Weng XY et al (2005) Leaf anatomy, chloroplast ultrastructure, and cellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) and RuBPCO activase in Amaranthus tricolor L. Photosynthetica 43(4):519–528

    Article  CAS  Google Scholar 

  • Huang D, Sun Y, Ma Z et al (2019) Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization. Proc Natl Acad Sci USA 116(42):21274–21284

    Article  CAS  Google Scholar 

  • Iswanto ABB, Kim JY (2017) Lipid raft, regulator of plasmodesmal callose homeostasis. Plants 6:15

    Article  Google Scholar 

  • Kriechbaumer V, Botchway S, Slade S et al (2015) Reticulomics: protein-protein interaction studies with two plasmodesmata-localized reticulon family proteins identify binding partners enriched at plasmodesmata, endoplasmic reticulum, and the plasma membrane. Plant Physiol 169:1933–1945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar R, Kumar D, Hyun TK et al (2015) Players at plasmodesmal nano-channels. J Plant Biol 58:75–86

    Article  CAS  Google Scholar 

  • Lee JY, Frank M (2018) Plasmodesmata in phloem: different gateways for different cargoes. Curr Opin Plant Biol 43:119–124

    Article  CAS  Google Scholar 

  • Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503

    Article  CAS  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17: No.1 (https://doi.org/10.14806/ej.17.1.200)

  • Mortazavi A, Williams BA, McCue K et al (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5(7):621

    Article  CAS  Google Scholar 

  • Murcia G, Pontin M, Piccoli P (2018) Role of ABA and Gibberellin A3 on gene expression pattern of sugar transporters and invertases in Vitis vinifera cv. Malbec during berry ripening. Plant Growth Regul 84:275–283

    Article  CAS  Google Scholar 

  • Nakajima K, Sena G, Nawy T et al (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  CAS  Google Scholar 

  • Nuñez C, Dupré G, Mujica K et al (2019) Thinning alters the expression of the PpeSUT1 and PpeSUT4 sugar transporter genes and the accumulation of translocated sugars in the fruits of an early season peach variety. Plant Growth Regul 88:283–296

    Article  Google Scholar 

  • Oparka KJ, Roberts AG, Boevink P et al (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754

    Article  CAS  Google Scholar 

  • Patro R, Duggal G, Love MI et al (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14(4):417

    Article  CAS  Google Scholar 

  • Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14:743–750

    Article  CAS  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139

    Article  CAS  Google Scholar 

  • Sager RE, Lee JY (2014) Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses. J Exp Bot 65:6337–6358

    Article  CAS  Google Scholar 

  • Sager RE, Lee JY (2018) Plasmodesmata at a glance. J Cell Sci 131:jcs209346.

  • Tilsner J, Nicolas W, Rosado A et al (2016) Staying tight: plasmodesmal membrane contact sites and the control of cell-to-cell connectivity in plants. Annu Rev Plant Biol 67:337–364

    Article  CAS  Google Scholar 

  • Stahl Y, Grabowski S, Bleckmann A et al (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23:362–371

    Article  CAS  Google Scholar 

  • Vaddepalli P, Herrmann A, Fulton L et al (2014) The C2-domain protein QUIRKY and the receptor-like kinase STRUBBELIG localize to plasmodesmata and mediate tissue morphogenesis in Arabidopsis thaliana. Development 141:4139–4148

    Article  CAS  Google Scholar 

  • Wang X, Sager R, Cui W et al (2013) Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:2315–2329

    Article  CAS  Google Scholar 

  • Wu SW, Kumar R, Iswanto ABB et al (2018) Callose balancing at plasmodesmata. J Exp Bot 69:5325–5339

    CAS  PubMed  Google Scholar 

  • Xu M, Cho E, Burch-Smith TM et al (2012) Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis. Proc Natl Acad Sci USA 109:5098–5103

    Article  CAS  Google Scholar 

  • Xu XM, Jackson D (2010) Lights at the end of the tunnel: new views of plasmodesmal structure and function. Curr Opin Plant Biol 13:684–692

    Article  CAS  Google Scholar 

  • Yadav RK, Perales M, Gruel J et al (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31801273, 31901346), the Zhejiang A&F University Scientific Research and Development Fund Project (2018FR049), the Department of Science and Technology of Ningbo (DSTNB, Project No. 2019C10008), and the China Postdoctoral Foundation (2016M591984).

Author information

Author notes

  1. Ying Yang and Xiaoting Xie have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin’an, Hangzhou, China

    Ying Yang, Xiaoting Xie, Shenchen Tao, Bingsong Zheng & Yi He

  2. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, China

    Kaiyue Zhou & Dean Jiang

  3. Hangzhou Runtu Horticulture Limited Company, Hangzhou, China

    Youxiang Yu

  4. Ulink College of Shanghai, Shanghai, China

    Zhe Lu

Authors
  1. Ying Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoting Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shenchen Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kaiyue Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Youxiang Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhe Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dean Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bingsong Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yi He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YH, BSZ and YYX contributed to the study conception and design. Material preparation was performed by YY, XTX, XCT and YXY. Data collection was performed by YY, XTX, KYZ and YH. Data analysis were performed by KYZ, ZL and YH. BSZ and YH wrote the manuscript, which was reviewed by DAJ. All co-authors read and approved this final manuscript.

Corresponding authors

Correspondence to Bingsong Zheng or Yi He.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 249 kb)

Supplementary file2 (DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Xie, X., Tao, S. et al. Plasmodesmata play a critical role in promoting the germination of floral buds in Ilex verticillata. Plant Growth Regul 91, 349–357 (2020). https://doi.org/10.1007/s10725-020-00609-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-020-00609-0

Keywords

Search

Navigation