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.
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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
`Navarro, C. et al. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478, 119–122 (2011).
Kloosterman, B. et al. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495, 246–250 (2013).
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).
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).
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).
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).
Bohlenius, H. et al. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312, 1040–1043 (2006).
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).
Tylewicz, S. et al. Photoperiodic control of seasonal growth is mediated by ABA acting on cell–cell communication. Science 360, 212–215 (2018).
Wang, M. et al. BRANCHED1: a key hub of shoot branching. Front. Plant Sci. 10, 76 (2019).
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).
Gonzalez-Grandio, E. et al. BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis. Plant Cell 25, 834–850 (2013).
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).
Maurya, J. P. et al. Branching regulator BRC1 mediates photoperiodic control of seasonal growth in hybrid aspen. Curr. Biol. 30, 122–126.e2 (2020).
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).
Martín-Trillo, M. et al. Role of tomato BRANCHED1-like genes in the control of shoot branching. Plant J. 67, 701–714 (2011).
Fernie, A. R. et al. Synchronization of developmental, molecular and metabolic aspects of source–sink interactions. Nat. Plants 6, 55–66 (2020).
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).
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).
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).
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).
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).
Singh, R. K. et al. A genetic network mediating the control of bud break in hybrid aspen. Nat. Commun. 9, 4173 (2018).
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).
Dong, Z. et al. The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression. Nat. Commun. 10, 3810 (2019).
González-Grandío, E. & Cubas, P. Identification of gene functions associated to active and dormant buds in Arabidopsis. Plant Signal. Behav. 9, e27994 (2014).
Nemhauser, J. L., Hong, F. & Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467–475 (2006).
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).
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).
Chen, H. Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol. 132, 1391–1404 (2003).
Sharma, P., Lin, T. & Hannapel, D. J. Targets of the StBEL5 transcription factor include the FT ortholog StSP6A. Plant Physiol. 170, 310–324 (2016).
Bolduc, N. et al. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26, 1685–1690 (2012).
Brault, M. L. et al. Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. EMBO Rep. 20, e47182 (2019).
Liu, L. et al. FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 10, e1001313 (2012).
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).
Viola, R. et al. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13, 385–398 (2001).
Knoblauch, M. et al. Multispectral phloem-mobile probes: properties and applications. Plant Physiol. 167, 1211–1220 (2015).
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).
Eviatar-Ribak, T. et al. A cytokinin-activating enzyme promotes tuber formation in tomato. Curr. Biol. 23, 1057–1064 (2013).
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).
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).
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).
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
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).
Yao, C. & Finlayson, S. A. Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth. Plant Physiol. 169, 611–626 (2015).
Ruttink, T. et al. A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19, 2370–2390 (2007).
Liu, L. et al. FTIP-dependent STM trafficking regulates shoot meristem development in Arabidopsis. Cell Rep. 23, 1879–1890 (2018).
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).
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).
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).
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).
Andrés, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627–639 (2012).
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).
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).
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).
Clement, K. et al. CRISPResso2 provides accurate and rapid genome editing sequence analysis. Nat. Biotechnol. 37, 224–226 (2019).
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).
Chevalier, F., Iglesias, S. M., Sánchez, O. J., Montoliu, L. & Cubas, P. Plastic embedding of stem sections. Bio-Protoc. 4, e1261 (2014).
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).
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).
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
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).
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).
Chen, C. et al. Real-time quantification of microRNAs by stem–loop RT–PCR. Nucleic Acids Res. 33, e179 (2005).
García-León, M. et al. Arabidopsis ALIX regulates stomatal aperture and turnover of abscisic acid receptors. Plant Cell 31, 2411–2429 (2019).
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).
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.
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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.
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Supplementary Data 1
RNA-seq data.
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PD gene expression.
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Primer list.
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Gene lists.
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Unprocessed western blots for Fig. 6b.
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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
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DOI: https://doi.org/10.1038/s41477-022-01112-2
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