Flowering in response to cold in annual and perennial plants

by Jens Sundström
Department of Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden.

In relation to annual plants, perennial plants initiate flowering after a more extended juvenile period. Also, perennial plants can often initiate flowering during repeated seasonable cycles and maintain vegetative shoot apical meristems during flowering. A recent study by Hyun and co-workers demonstrate that flowering in response to cold temperatures is regulated by distinct parallel pathways in the annual Arabidopsis thaliana and in the closely related perennial species Arabis alpina (Hyun et al., 2019).

In current discussions about future agriculture, perennial crops are frequently proposed as a possible solution for some of the problems associated with modern agriculture (Crews et al., 2018). In contrast to annual plants, which flower within one growing season, perennial plants typically go through a more extended juvenile period that may last several growth-seasons before flowering and seed production first is initiated. During the juvenile period, the plants invest in vegetative growth, which allows the plants to grow deeper root systems and more extensive foliage. Evergreen fields and plants with deeper root systems will increase carbon sequestration to the soil and provide crops with enhanced drought tolerance. Once the juvenile period has ended, perennial plants may go through repeated rounds flowering, which, if implemented in crop plants would allow for repeated harvesting without tillage, thus reducing nutrient leakage and fossil fuel usage. Hence, even though most crops presently are annuals, perenniality may become an important trait in future agriculture. Increased understanding of how annuals and perennials regulate flowering is therefore timely.

Figure 1. Schematic drawing on the genetic pathways regulating flowering in the annual Arabidopsis thaliana and in the perennial plant Arabis alpina (Illustration by Cajsa Lithell, RedCap design, 2019)

Described in general terms, the time to flower or flowering is determined by a combination of environmental and developmental signals. In temperate regions, an extended period of cold temperatures is often needed for flowering to occur, even if day-length and temperatures are permissive. This process is called vernalization, and in the annual crucifer A. thaliana winter temperatures lead to a stable down-regulation of the floral repressor FLOWERING LOCUS C (FLC) (Michaels and Amasino, 1999), which allows for flowering to occur when day length conditions are favourable (Figure 1). Studies of the perennial crucifer A. alpina have demonstrated that the FLC ortholog is only transiently down-regulated upon cold treatments (Wang et al., 2009), allowing for repeated cycles of floral initiation and floral repression, which is characteristic of the cyclic life history of perennials. 

One additional important distinction between annual and perennial plants is that in annuals all shoot meristems initiate reproductive development at the same time point, whereas perennial plants maintain vegetative after flower initiation. In perennial plants vegetative growth after flowering is maintained either by keeping some meristems in a vegetative state during flowering or by reverting meristems back to vegetative development after flowering.

In a recent study published in Science, Hyun and co-workers demonstrate that the characteristic perennial flowering properties of A. alpina depends on the floral integrator SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 15 (SPL15) (Hyun et al., 2019). In A. thaliana, SPL15 promotes flowering under short-day conditions. Using a combination of genetic and molecular methods, Hyun and co-workers showed that transcription of the SPL15 ortholog in A. alpina is negatively regulated by the FLC ortholog. Hence, temporal down-regulation of the FLC ortholog in shoot apical meristems in response to cold treatments leads to an up-regulation of AaSPL15 and subsequent flowering.

However, flowering is only initiated in shoot apical meristems of a certain age, suggesting an additional age-dependent regulation of AaSPL15. AaSPL15 belongs to a family of transcription factor-coding genes that are negatively regulated by microRNAs of the miR156 family. In diverse plant lineages, miR156 is expressed at high levels in young plants and the expression of miR156 gradually decreases as plants ages. miR156 binds to a specific motif in the AaSPL15 transcript, leading to a reduction in its levels (Bergonzi et al., 2013). By expressing a miR156-resistant form of AaSPL15 in transgenic A. alpina plants, Hyun and co-workers show that miR156 suppresses AsSPL15 accumulation in young shoot apical meristems. In line with this, cold-treated plants that express the miR156-resistant form of AaSPL15 display a shortened juvenile period and flower prematurely. In addition, shoot meristems that would be maintained as vegetative in the wild type initiate flowers in the transgenic plants, suggesting that AaSPL15 is negatively regulated by miR156 in an age-dependent manner.

Central to the seasonal reproductive cycles in A. alpina is the transient down-regulation of the FLC ortholog in response to cold (Wang et al., 2009). In the annual A. thaliana transcription of FLC is permanently down-regulated after cold treatment (Hepworth and Dean, 2015). FLC acts as a repressor of both SPL15 and genetic factors that promote flowering in response to day length. Hence, in the annual A. thaliana, long-day conditions after vernalization induce flowering, whereas restored expression of the FLC ortholog in A. alpina represses flowering in response to day length conditions.

Taken together, this suggests that AaSPL15 integrates cues derived from winter cold and age in shoot apical meristems of A. alpina. The transient down-regulation of the FLC ortholog in A. alpina and subsequent up-regulation of AaSPL15 transcription allows for seasonal induction of flowering after winter vernalization, whereas expression of miR156 suppresses AaSPL15 in juvenile plants and in meristems that maintain vegetative identity during flowering.

Distinctions between annual and perennial growth have arisen independently in many different plant lineages (Thomas et al., 2000), suggesting that distinct mechanisms may regulate flowering in different plant lineages. However, the central genetic components of the flowering pathways are in many cases well conserved even between distantly related plant lineages indicating that it is, in part, the regulation of the flowering pathways that determine an annual or perennial life cycle. It will be interesting to see if the knowledge gained in these studies can facilitate further development of perennial crops plants.

References

Bergonzi S, Albani MC, Ver Loren van Themaat E, Nordstrom KJ, Wang R, Schneeberger K, Moerland PD, Coupland G. 2013. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340, 1094-1097. DOI: 10.1126/science.1234116

Crews TE, Carton W, Olsson L. 2018. Is the future of agriculture perennial? Imperatives and opportunities to reinvent agriculture by shifting from annual monocultures to perennial polycultures. Global Sustainability 1, e11. https://doi.org/10.1017/sus.2018.11

Hepworth J, Dean C. 2015. Flowering locus C’s lessons: conserved chromatin switches underpinning developmental timing and adaptation. Plant Physiology 168, 1237-1245. DOI: https://doi.org/10.1104/pp.15.00496

Hyun Y, Vincent C, Tilmes V, Bergonzi S, Kiefer C, Richter R, Martinez-Gallegos R, Severing E, Coupland G. 2019. A regulatory circuit conferring varied flowering response to cold in annual and perennial plants. Science 363, 409-412. DOI: 10.1126/science.aau8197

Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956. DOI: https://doi.org/10.1105/tpc.11.5.949

Thomas H, Thomas HM, Ougham H. 2000. Annuality, perenniality and cell death. Journal of Experimental Botany 51, 1781-1788.
https://doi.org/10.1093/jexbot/51.352.1781

Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC. 2009. PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423-427. https://doi.org/10.1038/nature07988

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About Flowering Highlights

Flowering Newsletter published by the Journal of Experimental Botany
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