The cultivation of perennial crops offers significant potential for sustainable agriculture. In 2022, the development of perennial rice was highlighted as the world’s second top scientific breakthroughs by
Science magazine. It is generally believed that perennial plants are more ancient, and annual plants have evolved from perennials. However, the genetic basis of the evolutionary transition from perennial to biennial and annual plants is still poorly understood.
In a study published online in
Cell, a research group led by Dr. WANG Jiawei at the Center for Excellence in Molecular Plant Sciences of the Chinese Academy of Sciences
implemented reciprocal conversion between annual and polycarpic perennial flowering behavior in Brassicaceae.Using plant genera with rich variation in life-history strategies as models, researchers identified three MADS-box genes determining the evolution of plant life-history strategies (i.e., polycarpic perennial flowering behavior) by constructing cross-species mapping populations and operating forward genetics approaches. They revealed that the dosage effects of these three genes determined the evolutionary trajectories of plant life-history strategies. Remarkably, a single gene among these three was sufficient to convert annual plants into polycarpic perennial flowering plants.
To reveal the genetic basis of the evolutionary transition between perenniality and annuality, researchers selected two pairs of compatible annual/perennial plant combinations from the Brassicaceae family. Within the Crucihimalaya genus, Crucihimalaya himalaica is a polycarpic perennial, whereas Crucihimalaya wallichii exhibits facultative winter annual/polycarpic perennial characteristics. In the Erysimum genus, Erysimum nevadense is a polycarpic perennial, and Erysimum cheiranthoides is an annual.
Using the two mapping populations with distinct life-history phenotypes from these four plants, researchers identified three genetic regions associated with the evolution of life-history strategies. According to the gene functional annotations of the model plant Arabidopsis thaliana, they identified three closely related MADS-box transcription factor genes, namely FLOWERING LOCUS C (FLC), FLOWERING LOCUS M (FLM) and MADS AFFECTING FLOWERING (MAF).
To further confirm the mapping results, FLC, FLM, and MAF loci in Crucihimalaya plants were mutated using CRISPR/Cas9 technology. By combining mutant alleles in different combinations through crossing, researchers recapitulated the evolutionary trajectory of plants transitioning from polycarpic perennial to biennial and annual. They found that when FLC, FLM, MAF all remain functionally intact, the plant exhibits a robust polycarpic perennial phenotype, the absence of one or two of these genes leads to the adoption of facultative life-history strategies, and when all these genes are completely inactive, the plant transitions to annual flowering growth habit.
Through RNA-seq and H3K27me3 ChIP-seq experiments on the parental and F1 generation plants, researchers observed that FLC-like MADS-box genes in annual E. cheiranthoides tend to be stably repressed after vernalization, whereas homologous genes from perennial E. nevadense tend to be reset after vernalization. This difference constituted the molecular basis underlying the establishment of polycarpic perennial life-history strategy and was determined by the specific sequences of the genes themselves. Notably, while FLC, FLM and MAF have close genetic relationships, they differ in terms of gene function, expression levels, as well as the timing and intensity of resetting.
Based on the above results, researchers proposed how the life-history strategies in Brassicaceae are evolved. Specifically, the transition among perennial, biennial, and annual flowering behavior is a continuum and determined by gene dosage effects of FLC-like MADS-box genes. The diversity of these genes in expression patterns, protein functions and epigenetic resetting modes, as well as their different combinations, allows plants to have a wide range of life-history strategies to adapt to diverse environmental conditions.
By introducing a perennial FLC gene into annual A. thaliana, researchers transformed A. thaliana from monocarpic annual to polycarpic perennial. This result suggested that A. thaliana has the prerequisite conditions of being polycarpic perennial. Perennial FLC-like MADS-box genes are likely necessary and sufficient for the establishment of polycarpic perennial life-history strategy. This result also lays the foundation for future cultivation of polycarpic perennial Brassica napus.
