Geminivirus-Mediated Delivery of Florigen Promotes Determinate Growth in Aerial Organs and Uncouples Flowering from Photoperiod in Cotton

Abstract

BackgroundPlant architecture and the timing and distribution of reproductive structures are fundamental agronomic traits shaped by patterns of determinate and indeterminate growth. Florigen, encoded by FLOWERING LOCUS T (FT) in Arabidopsis and SINGLE FLOWER TRUSS (SFT) in tomato, acts as a general growth hormone, advancing determinate growth. Domestication of upland cotton (Gossypium hirsutum) converted it from a lanky photoperiodic perennial to a highly inbred, compact day-neutral plant that is managed as an annual row-crop. This dramatic change in plant architecture provides a unique opportunity to analyze the transition from perennial to annual growth.Methodology/Principal FindingsTo explore these architectural changes, we addressed the role of day-length upon flowering in an ancestral, perennial accession and in a domesticated variety of cotton. Using a disarmed Cotton leaf crumple virus (CLCrV) as a transient expression system, we delivered FT to both cotton accessions. Ectopic expression of FT in ancestral cotton mimicked the effects of day-length, promoting photoperiod-independent flowering, precocious determinate architecture, and lanceolate leaf shape. Domesticated cotton infected with FT demonstrated more synchronized fruiting and enhanced “annualization”. Transient expression of FT also facilitated simple crosses between wild photoperiodic and domesticated day-neutral accessions, effectively demonstrating a mechanism to increase genetic diversity among cultivated lines of cotton. Virus was not detected in the F1 progeny, indicating that crosses made by this approach do not harbor recombinant DNA molecules.ConclusionsThese findings extend our understanding of FT as a general growth hormone that regulates shoot architecture by advancing organ-specific and age-related determinate growth. Judicious manipulation of FT could benefit cotton architecture to improve crop management.

Virus-Induced Flowering: An Application of Reproductive Biology to Benefit Plant Research and Breeding

“…In both cases, the F1 progeny displayed phenotypes intermediate to both parents, demonstrating the success of the cross. Importantly, neither dCLCrV nor ALSV was detected in the F1 generation McGarry and Ayre, 2012b).…”

“…This early work demonstrated that FT encoded florigenic properties and laid the foundation for VIF as a breeding tool. Work in cotton demonstrated that ectopic expression of AtFT from a disarmed Cotton leaf crumple virus (dCLCrV) vector uncoupled flowering from photoperiod, accelerated the transition to reproductive growth, and enhanced determinate plant architecture (McGarry and Ayre, 2012b). Ectopic expression of AtFT in soybean (Glycine max) with both determinate or indeterminate stem habits, when delivered by Apple latent spherical virus (ALSV), terminated vegetative growth without an inductive short-day treatment .…”

“…VIF using AtFT or cotton SINGLE FLOWER TRUSS (GhSFT; SFT is the FT ortholog in tomato [Solanum lycopersicum]) gain of function rapidly induced the onset of flowering, and growth was more determinate than in naturally reproductive plants (Fig. 2, B and C;McGarry and Ayre, 2012b;McGarry et al, 2016). However, VIGS of SELF-PRUNING (GhSP; a tomato homolog of TFL1) using Tobacco rattle virus (TRV) more severely altered growth habit.…”

A Virus-Induced Assay for Functional Dissection and Analysis of Monocot and Dicot Flowering Time Genes

“…Plants respond to such biotic stresses by speeding up their reproductive process to flower earlier. This could complicate the interpretation of results of VIFs, such as those based on Zucchini yellow mosaic virus, Cotton leaf crumple virus, or Citrus leaf blotch virus, because all these viruses produced severe systemic symptoms in viral-infected plants (Lin et al, 2007;McGarry and Ayre, 2012;Velázquez et al, 2016). However, the PVX-infected tobacco plants exhibited normal vegetative and reproductive growth (Fig.…”

“…These findings open up possibilities for further development and application of the virus-induced flowering (VIF) assay in plants (McGarry et al, 2017). Since then, several RNA and DNA viruses, including Apple latent spherical virus, Cotton leaf crumple virus, and Citrus leaf blotch virus, have been engineered to express FT for floral induction in soybean, apple, pear, gentian, and lisianthus plants Yamagishi et al, , 2014Yamagishi et al, , 2016Fekih et al, 2016), cotton (McGarry andAyre, 2012;McGarry et al, 2016), and citrus (Velázquez et al, 2016). These latest developments have generated broad interest in the application of VIF for the benefit of crop breeding (McGarry et al, 2017).…”