Late bloomers: subtle diversity in flowering time

How do plants know when to start flowering? What are the mechanisms underlying flowering diversity? We identified a natural polymorphism in CONSTANS, a regulatory gene controlling the flowering time developmental transition in Arabidopsis. We found that the polymorphism in CONSTANS controls transcriptional variation and flowering time diversity in Arabidopsis thaliana populations. This is one of the few natural regulatory polymorphisms known in Arabidopsis and other plants to be widely spread in populations.

HFSP Long-Term Fellow Ulises Rosas and colleagues
authored on Tue, 13 May 2014

Like many other organisms, plants have mechanisms to determine when to invest their resources in crucial developmental transitions. One of the most important developmental transitions in plants is the initiation of flowering. In the model plant Arabidopsis thaliana, we have a good understanding of the main genetic and molecular players controlling the flowering time developmental transition. Moreover, we also know that Arabidopsis thaliana natural populations have a wide distribution in most of Europe and Asia, and are exposed to a wide variety of environmental conditions. Thus, local adaptation might be expected in each population, as the flowering time developmental machinery is tuned according to the requirements of the environment. Nevertheless, to date we only know a handful of genes responsible for diversity in flowering time. Moreover, most of the known examples might be rare alleles present in a few Arabidopsis thaliana populations.   

Figure: Variation in the regulatory sequence of CONSTANS (CO). Water color and composition: Claudia L. Arana-Coronado.

In a recent study, our collaborative team led by Prof Michael Purugganan (New York University), and Prof Yoshie Hanzawa (University of Illinois) shed light on the subject. We investigated an important gene controlling the flowering time reproductive transition called CONSTANS. In a previous study, Dr Hanzawa characterized the sequence variation (or polymorphisms) in the flowering time developmental network using several Arabidopsis thaliana populations and found a number of polymorphisms. Some gave structural changes in the CONSTANS protein while others occurred in regulatory sequences that control when, where, and how much CONSTANS protein is produced. Most of these polymorphisms were rare or present in just a few Arabidopsis thaliana populations, which suggested their minor role in evolution and diversification in flowering time. However, one regulatory polymorphism was present in a large pool of Arabidopsis thaliana populations. This was a tandem repeat of seven nucleotides, containing the four nucleotide binding site of a repressor of CONSTANS. 60% of the populations had three times the repeat (3X), whereas 40% of the populations had a four times the repeat (4X). This led our team to ask: did the 3X/4X polymorphism arise recently and spread through the populations? Does the 3X/4X polymorphism affect the activity of CONSTANS? And most importantly, is the 3X/4X polymorphism responsible for diversity in flowering time in Arabidopsis thaliana populations?   

To address these questions, our team studied the CONSTANS sequences associated to the 3X/4X polymorphism, showing that the 4X allele had a more recent origin than the 3X allele. The two types of sequences were isolated and fused to a standard CONSTANS gene and transformed into Arabidopsis thaliana. When measuring the flowering time of the transgenic lines, we found that plants with the 4X allele flowered later than plants with the 3X allele, demonstrating that the 3X/4X natural polymorphism is responsible for variation in flowering time. We also attributed the differences in flowering time to variation in CONSTANS transcriptional activity due to the 3X/4X alleles.

In summary, in CONSTANS, a regulatory polymorphism originated recently, giving differences in CONSTANS transcription, and is responsible for subtle diversity in flowering time in Arabidopsis populations: the higher the number of repeats, the longer it takes for the plant to flower. These findings will open avenues of research for the potential use of the CONSTANS regulatory polymorphism to engineer the flowering time in Arabidopsis and related crop species. This is one of the few examples of a high frequency regulatory polymorphism controlling the diversity of a major developmental event in plants.


Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS. Ulises Rosas, Yu Mei, Qiguang Xie, Joshua A. Banta, Royce W. Zhou, Gabriela Seufferheld, Silvia Gerard, Lucy Chou, Naeha Bhambhra, Jennifer Deane Parks, Jonathan M. Flowers, C. Robertson McClung, Yoshie Hanzawa, & Michael D. Purugganan. Nature Communications 5, Article number 3651, doi:10.1038/ncomms4651.

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