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 CO 2 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 cold temperatures and animal foraging. We show that BRANCHED1b (BRC1b) acts as a tuberisation 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 tuberisation. In buds, BRC1b promotes dormancy, ABA signalling and downregulation of plasmodesmata gene expression. This limits sucrose unloading and access of the tuberigen factor SP6A to axillary buds. Moreover, BRC1b directly interacts with SP6A and blocks its tuber-forming activity in aerial nodes. Altogether these actions help promote tuberisation underground.A central question in plant biology is how carbon partitioning is regulated in response to changing environmental conditions, and how this control is integrated with developmental programs. Plant meristems, groups of undifferentiated, actively dividing cells, are sink organs that use sucrose for respiration, growth and development. Under low sucrose availability, they remain quiescent or dormant. Axillary meristems, shoot meristems located in the leaf axils, can give rise to aerial branches with orthotropic growth that produce leaves, inflorescences and flowers. They can also generate stolons, specialised shoots, homologous to branches, that grow horizontally on the soil surface or below ground and have the potential to generate new clonal plants, thus being strategic for vegetative propagation. Branches and stolons differ in their developmental responses to external stimuli, such as day length (see below).Solanum tuberosum (potato) is one of the best-studied stolon-forming species, as their underground stolons develop energy-rich, starch-accumulating tubers, which constitute a large fraction of the dietary intake for many people worldwide. In the potato landrace ssp. andigena, the stolons become strong sinks when winter approaches, and form tubers at their sub-apical region. Tubers overwinter buried in soil, where they are protected from cold and animal foraging, to generate entirely new plants in spring.Tuberisation is controlled by the FLOWERING LOCUS T (FT)-like SELF-PRUNING 6A (SP6A) gene. In potato ssp. andigena, activation of this gene is fully dependent on short days (SD). In long days (LD), the CONSTANS-like1 (COL1) transcription factor represses SP6A expression through the activation of another FT-like gene, SP5G 1,2 . In SD, lack of SP5G allows SP6A activation, and the SP6A protein is then phloem-transported from leaves to stolons. At the stolon apices, SP6A form a Tuberigen Activation Complex (TAC) that acts to promote tuber formation 3,4 .Unlike stolons, neither branches nor branch primordia, namely axillar...

Profiling of the Candidate Interacting Proteins of SELF-PRUNING 6A (SP6A) in Solanum tuberosum

“…However, the molecular mechanism of flowering and branching remains elusive. Some proteins interacting with StSP6A have been reported, including StFDL1, StABL1, StSWEET11, and BRC1b [ 6 , 7 , 8 , 9 , 11 ]. It is important to explore whether there are some other unknown StSP6A interactors involved in other functions.…”

“…In potato, StSP6A interacts with the SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER 11 (StSWEET11) to promote the symplastic transport of sucrose to affect the source-sink pathway of tuberization [ 8 ]. It has been also reported that StSP6A is involved in branching and flowering [ 9 , 10 ]. A TCP transcription factor, BRANCHED1b (BRC1b), interacts with StSP6A to promote dormancy and repress tuberization [ 9 , 11 ].…”

“…It has been also reported that StSP6A is involved in branching and flowering [ 9 , 10 ]. A TCP transcription factor, BRANCHED1b (BRC1b), interacts with StSP6A to promote dormancy and repress tuberization [ 9 , 11 ]. Under SD conditions, the development of flower buds is repressed by the tuberization signal StSP6A [ 10 ].…”

Global transcriptome and coexpression network analyses reveal cultivar-specific molecular signatures associated with different rooting depth responses to drought stress in potato

“…Root depth (deep or shallow) is an important agronomic trait related to yield potential and is particularly important in potato tubers ( Xu et al., 2017 ; Wang et al., 2020b ). In potato tubers, root development begins at tuber germination, and the first young buds appear with scaly or “embryo” leaves at the top, followed by young roots on several sections at the base of the buds ( Nicolas et al., 2022 ). The early period is primarily for root formation and bud growth, which form the basis for tuber seedling rooting, tuber formation, and plant strengthening ( Zhou et al., 2017 ; Omary et al., 2022 ).…”

Addendum: Genome evolution and diversity of wild and cultivated potatoes

“…After our manuscript was accepted in principle, a study by Nicolas et al 1 showed that BRANCHED1b acts as a tuberization repressor in aerial axillary buds in tetraploid potato. We note that IT1 and BRANCHED1b are the same gene.…”