Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Spatial control of potato tuberization by the TCP transcription factor BRANCHED1b

Abstract

The control of carbon allocation, storage and usage is critical for plant growth and development and is exploited for both crop food production and CO2 capture. Potato tubers are natural carbon reserves in the form of starch that have evolved to allow propagation and survival over winter. They form from stolons, below ground, where they are protected from adverse environmental conditions and animal foraging. We show that BRANCHED1b (BRC1b) acts as a tuberization repressor in aerial axillary buds, which prevents buds from competing in sink strength with stolons. BRC1b loss of function leads to ectopic production of aerial tubers and reduced underground tuberization. In aerial axillary buds, BRC1b promotes dormancy, abscisic acid responses and a reduced number of plasmodesmata. This limits sucrose accumulation and access of the tuberigen protein SP6A. BRC1b also directly interacts with SP6A and blocks its tuber-inducing activity in aerial nodes. Altogether, these actions help promote tuberization underground.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Expression of BRC1b during potato (ssp. andigena) development.
Fig. 2: Aerial tuber phenotype of potato (ssp. andigena) BRC1b RNAi lines.
Fig. 3: Sucrose content and symplasmic transport in BRC1b RNAi lines.
Fig. 4: Transcriptomic changes in BRC1b RNAi buds.
Fig. 5: BRC1b RNAi axillary buds have more PD than WT in SD.
Fig. 6: BRC1b interacts with SP6A in yeast and in planta.
Fig. 7: Model for the role of BRC1b in potato axillary buds.

Similar content being viewed by others

Data availability

The RNA-seq data generated in this study have been deposited in the Gene Expression Omnibus under accession no. GSE155774. Source data are provided with this paper.

References

  1. `Navarro, C. et al. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478, 119–122 (2011).

    Article  CAS  Google Scholar 

  2. Kloosterman, B. et al. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495, 246–250 (2013).

    Article  CAS  PubMed  Google Scholar 

  3. Abelenda, J. A., Cruz-Oró, E., Franco-Zorrilla, J. M. & Prat, S. Potato StCONSTANS-like1 suppresses storage organ formation by directly activating the FT-like StSP5G repressor. Curr. Biol. 26, 872–881 (2016).

    Article  CAS  PubMed  Google Scholar 

  4. Teo, C.-J., Takahashi, K., Shimizu, K., Shimamoto, K. & Taoka, K. Potato tuber induction is regulated by interactions between components of a tuberigen complex. Plant Cell Physiol. 58, 365–374 (2017).

    CAS  PubMed  Google Scholar 

  5. Tarancón, C., González-Grandío, E., Oliveros, J. C., Nicolas, M. & Cubas, P. A conserved carbon starvation response underlies bud dormancy in woody and herbaceous species. Front. Plant Sci. 8, 788 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Martín-Fontecha, E. S., Tarancón, C. & Cubas, P. To grow or not to grow, a power-saving program induced in dormant buds. Curr. Opin. Plant Biol. 41, 102–109 (2018).

    Article  PubMed  Google Scholar 

  7. Bohlenius, H. et al. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040–1043 (2006).

    Article  PubMed  CAS  Google Scholar 

  8. Rinne, P. L. H., Kaikuranta, P. M. & Van Schoot, C. Der The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J. 26, 249–264 (2001).

    Article  CAS  PubMed  Google Scholar 

  9. Tylewicz, S. et al. Photoperiodic control of seasonal growth is mediated by ABA acting on cell–cell communication. Science 360, 212–215 (2018).

    Article  CAS  PubMed  Google Scholar 

  10. Wang, M. et al. BRANCHED1: a key hub of shoot branching. Front. Plant Sci. 10, 76 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Aguilar-Martínez, J. A., Poza-Carrión, C. & Cubas, P. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19, 458–472 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Gonzalez-Grandio, E. et al. BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis. Plant Cell 25, 834–850 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. González-Grandío, E. et al. Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds. Proc. Natl Acad. Sci. USA 114, E245–E254 (2017).

    Article  PubMed  CAS  Google Scholar 

  14. Maurya, J. P. et al. Branching regulator BRC1 mediates photoperiodic control of seasonal growth in hybrid aspen. Curr. Biol. 30, 122–126.e2 (2020).

    Article  CAS  PubMed  Google Scholar 

  15. Nicolas, M., Rodríguez-Buey, M. L. L., Franco-Zorrilla, J. M. M. & Cubas, P. A recently evolved alternative splice site in the BRANCHED1a gene controls potato plant architecture. Curr. Biol. 25, 1799–1809 (2015).

    Article  CAS  PubMed  Google Scholar 

  16. Martín-Trillo, M. et al. Role of tomato BRANCHED1-like genes in the control of shoot branching. Plant J. 67, 701–714 (2011).

    Article  PubMed  CAS  Google Scholar 

  17. Fernie, A. R. et al. Synchronization of developmental, molecular and metabolic aspects of source–sink interactions. Nat. Plants 6, 55–66 (2020).

    Article  PubMed  Google Scholar 

  18. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Campbell, M., Suttle, J., Douches, D. S. & Buell, C. R. Treatment of potato tubers with the synthetic cytokinin 1-(α-ethylbenzyl)-3-nitroguanidine results in rapid termination of endodormancy and induction of transcripts associated with cell proliferation and growth. Funct. Integr. Genomics 14, 789–799 (2014).

    Article  CAS  PubMed  Google Scholar 

  20. Gonzali, S. et al. Identification of sugar-modulated genes and evidence for in vivo sugar sensing in Arabidopsis. J. Plant Res. 119, 115–123 (2006).

    Article  CAS  PubMed  Google Scholar 

  21. Osuna, D. et al. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J. 49, 463–491 (2007).

    Article  CAS  PubMed  Google Scholar 

  22. Paul, L. K., Rinne, P. L. H. & van der Schoot, C. Shoot meristems of deciduous woody perennials: self-organization and morphogenetic transitions. Curr. Opin. Plant Biol. 17, 86–95 (2014).

    Article  PubMed  Google Scholar 

  23. Singh, R. K. et al. A genetic network mediating the control of bud break in hybrid aspen. Nat. Commun. 9, 4173 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Karlberg, A. et al. Analysis of global changes in gene expression during activity–dormancy cycle in hybrid aspen apex. Plant Biotechnol. 27, 1–16 (2010).

    Article  CAS  Google Scholar 

  25. Dong, Z. et al. The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression. Nat. Commun. 10, 3810 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. González-Grandío, E. & Cubas, P. Identification of gene functions associated to active and dormant buds in Arabidopsis. Plant Signal. Behav. 9, e27994 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Nemhauser, J. L., Hong, F. & Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467–475 (2006).

    Article  CAS  PubMed  Google Scholar 

  28. Abelenda, J. A. et al. Source–sink regulation is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr. Biol. 29, 1178–1186.e6 (2019).

    Article  CAS  PubMed  Google Scholar 

  29. Kloosterman, B. et al. StGA2ox1 is induced prior to stolon swelling and controls GA levels during potato tuber development. Plant J. 52, 362–373 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. Chen, H. Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol. 132, 1391–1404 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sharma, P., Lin, T. & Hannapel, D. J. Targets of the StBEL5 transcription factor include the FT ortholog StSP6A. Plant Physiol. 170, 310–324 (2016).

    Article  CAS  PubMed  Google Scholar 

  32. Bolduc, N. et al. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26, 1685–1690 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Brault, M. L. et al. Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. EMBO Rep. 20, e47182 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Liu, L. et al. FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 10, e1001313 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Song, S. et al. OsFTIP1-mediated regulation of florigen transport in rice is negatively regulated by the ubiquitin-like domain kinase OsUbDKγ4. Plant Cell 29, 491–507 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Viola, R. et al. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13, 385–398 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Knoblauch, M. et al. Multispectral phloem-mobile probes: properties and applications. Plant Physiol. 167, 1211–1220 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Niwa, M. et al. BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25, 1228–1242 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Eviatar-Ribak, T. et al. A cytokinin-activating enzyme promotes tuber formation in tomato. Curr. Biol. 23, 1057–1064 (2013).

    Article  CAS  PubMed  Google Scholar 

  40. Kumar, A., Kondhare, K. R., Vetal, P. V. & Banerjee, A. K. PcG proteins MSI1 and BMI1 function upstream of miR156 to regulate aerial tuber formation in potato. Plant Physiol. 182, 185–203 (2020).

    Article  CAS  PubMed  Google Scholar 

  41. Bhogale, S. et al. MicroRNA156: a potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiol. 164, 1011–1027 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Lu, Z. et al. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture. Plant Cell 25, 3743–3759 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Nicolas, M. & Cubas, P. in Plant Transcription Factors (ed. Gonzalez, D. H.) 249–267 (Elsevier, 2016); https://doi.org/10.1016/B978-0-12-800854-6.00016-6

  44. Reddy, S. K., Holalu, S. V., Casal, J. J. & Finlayson, S. A. Abscisic acid regulates axillary bud outgrowth responses to the ratio of red to far-red light. Plant Physiol. 163, 1047–1058 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yao, C. & Finlayson, S. A. Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth. Plant Physiol. 169, 611–626 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ruttink, T. et al. A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19, 2370–2390 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Liu, L. et al. FTIP-dependent STM trafficking regulates shoot meristem development in Arabidopsis. Cell Rep. 23, 1879–1890 (2018).

    Article  CAS  PubMed  Google Scholar 

  48. Vaddepalli, P. et al. 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 (2014).

    Article  CAS  PubMed  Google Scholar 

  49. Ho, L. C. Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 355–378 (1988).

    Article  CAS  Google Scholar 

  50. Xu, X., van Lammeren, A. A., Vermeer, E. & Vreugdenhil, D. The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol. 117, 575–584 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pasare, S. A. et al. The role of the potato (Solanum tuberosum) CCD8 gene in stolon and tuber development. N. Phytol. 198, 1108–1120 (2013).

    Article  CAS  Google Scholar 

  52. Andrés, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627–639 (2012).

    Article  PubMed  CAS  Google Scholar 

  53. Maurya, J. P. & Bhalerao, R. P. Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: a molecular perspective. Ann. Bot. 120, 351–360 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Nakagawa, T. et al. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34–41 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Fauser, F., Schiml, S. & Puchta, H. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79, 348–359 (2014).

    Article  CAS  PubMed  Google Scholar 

  56. Clement, K. et al. CRISPResso2 provides accurate and rapid genome editing sequence analysis. Nat. Biotechnol. 37, 224–226 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Seibert, T., Abel, C. & Wahl, V. Flowering time and the identification of floral marker genes in Solanum tuberosum ssp. andigena. J. Exp. Bot. 71, 986–996 (2020).

    Article  CAS  PubMed  Google Scholar 

  58. Chevalier, F., Iglesias, S. M., Sánchez, O. J., Montoliu, L. & Cubas, P. Plastic embedding of stem sections. Bio-Protoc. 4, e1261 (2014).

    Article  Google Scholar 

  59. Chen, Y. et al. SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. Gigascience 7, gix120 (2018).

    Article  Google Scholar 

  60. Sharma, S. K. et al. Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. G3 (Bethesda) 3, 2031–2047 (2013).

    Article  PubMed Central  CAS  Google Scholar 

  61. Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Liao, Y., Smyth, G. K. & Shi, W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 47, e47 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Chen, C. et al. Real-time quantification of microRNAs by stem–loop RT–PCR. Nucleic Acids Res. 33, e179 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. García-León, M. et al. Arabidopsis ALIX regulates stomatal aperture and turnover of abscisic acid receptors. Plant Cell 31, 2411–2429 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Nieto, C., López-Salmerón, V., Davière, J. & Prat, S. ELF3–PIF4 interaction regulates plant growth independently of the evening complex. Curr. Biol. 25, 187–193 (2015).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work of P.C. was funded by BIO2014-57011-R (MINECO), BIO2017-84363-R (Spanish Ministry of Science and Innovation) (MCIN/AEI/10.13039/501100011033/) and FESF investing in your future. The work of S.P. was funded by BIO2015-73019-EXP (Spanish Ministry of Science and Innovation) (MCIN/AEI/10.13039/501100011033/), ERA-NET COSMIC EIG CONCERT-Japan (PCIN-2017-032) (Spanish Ministry of Science and Innovation) and European Union H2020 ‘ADAPT’ project. The work of R.T.-P. and J.C.O. was funded by CSIC-202020E079 (Spanish National Research Council). The work of V.W. was funded by BMBF (031B0191), DFG (SPP1530: WA3639/1-2, 2-1) and Max-Planck-Society. M.N. had an Excellence Severo Ochoa contract (MINECO, SEV-2013-0347). The CNB is a Severo Ochoa Center of Excellence (MINECO award SEV 2017-0712). We thank T. Seibert for help with in situ hybridizations and photography, L. Yan for amplicon sequencing of the brc1b CRISPR lines, I. Poveda for the photographs of aerial tubers and D. Bradley and J. A. Abelenda for constructive criticisms of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

M.N., S.P. and P.C. designed the research. M.N., V.W., M.L.R.-B., E.C.-O., A.M.Z., J.M.G.-M., B.M.-J., S.P. and P.C. performed the research. R.T.-P. and J.C.O. analysed data. M.N. and P.C. wrote the article.

Corresponding authors

Correspondence to Michael Nicolas or Pilar Cubas.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Plants thanks Christian Bachem, Uwe Sonnewald and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Figs. 1–10.

Reporting Summary

Supplementary Data 1

RNA-seq data.

Supplementary Data 2

PD gene expression.

Supplementary Data 3

Primer list.

Supplementary Data 4

Gene lists.

Source data

Source Data Fig. 6

Unprocessed western blots for Fig. 6b.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nicolas, M., Torres-Pérez, R., Wahl, V. et al. Spatial control of potato tuberization by the TCP transcription factor BRANCHED1b. Nat. Plants 8, 281–294 (2022). https://doi.org/10.1038/s41477-022-01112-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-022-01112-2

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing