Ferns are one of the final frontiers in plant genomics. The dearth of fern genomic resources is due primarily to their notoriously high chromosome numbers and large genome sizes—ferns can have chromosome numbers as high as 2n=1440, and genome sizes as high as 1C=71 Gb (>470 times larger than Arabidopsis). However, we have recently discovered that Azolla and Salvinia (two closely related aquatic fern genera) have the smallest fern genomes known to date (0.75 Gb and 0.25 Gb respectively), while the average fern genome size is over 12 Gb. We have already assembled and annotated the whole genomes of Azolla filiculoides and Salvinia cucullata.
These first fern genomes will make possible many exciting research opportunities. We are interested in examining the patterns of paleopolyploidization, genome expansion/contraction, as well as transposable element activities in ferns, and contrast them across other plant genomes. We are also curious about how gene family evolution—particularly those that play critical roles in reproduction and development—influences the origin and evolution of plant life forms. Finally, we are keen to find out what drove the remarkable variation in both genome size and chromosome number across land plants.
Hornworts as a new model system
Hornworts are one of the three bryophyte lineages (together with mosses and liverworts), and have a suite of fascinating biological features. For example, some hornwort species have a unique carbon-concentration mechanism to boost photosynthesis, like C4 or CAM but at the single-cell level. In addition, every single hornwort species are capable to form symbiosis with cyanobacteria, and thus hold the key to understand plant interactions with nitrogen-fixing microbes.
Working with Juan Carlos Villarreal at Laval University, Peter Szoevenyi at University of Zurich, and Shifeng Cheng at BGI, we have assembled complete genomes from three hornwort species. We have also been developing tools for genetic transformation as well as CRISPR-Cas9 genome editing to enable reverse genetic interrogation in hornworts. We hope to apply these tools and genomic resources to tackle various research questions, from the origin of cyanobacteria symbiosis to the evolution of plant body plans.
Plant-bacterial symbiosis is a major driver in evolution, and its role in nitrogen fixation is particularly important in agriculture. Past studies of plant-bacteria interactions have focused primarily on the legume-Rhizobium system. Although significant, this particular symbiosis has had only a single evolutionary origin, thus limiting its utility as a model for understanding the genetic mechanisms underlying other symbiotic plant-bacteria partnerships. In contrast, symbioses with the other group of nitrogen-fixing bacteria––the cyanobacteria—have independently evolved multiple times, in liverworts, hornworts, ferns (i.e. Azolla), cycads, and flowering plants.
We aim to leverage the power of such convergent evolution––independently evolved in each of these disparate plant groups––to identify the genetic commonalities that were repeatedly recruited to assemble this mutually-beneficial association. Specifically, we will be looking for signatures of convergent evolution at the genome, gene and amino acid levels. At the genome level, we will focus on concerted gene family expansion or contraction, loss or retention of metabolic pathways, proliferation or purging of transposable elements, and horizontal gene transfer between cyanobacteria and plants. At the gene level, we will identify genes that exhibit similar expression profiles when a cyanobacterial symbiosis is present versus absent. And at the amino acid levels, we will reconstruct gene phylogenies for all orthologous genes and examine if similar, positively- selected amino acid substitutions occurred each time a symbiotic event evolved. The genetic elements identified through this comparative genomic analysis will be instrumental for engineering artificial nitrogen-fixing symbiosis onto crop plants.
Plant photoreceptor evolution
“Light exerts a powerful influence on most vegetable tissues, and there can be no doubt that it generally tends to check their growth” – Charles Darwin, 1880
Light is the ultimate source of energy for much of life on earth, and inevitably governs the growth and physiology of photosynthetic organisms. Plants “see” light through photoreceptors. To understand how plants adapted to, and thrived in, the diverse environments they inhabit, the roles of photoreceptors cannot be ignored. Our research has been focusing on neochrome, a bizarre chimeric photoreceptor that fuses red-sensing phytochrome and blue-sensing phototropin together in a single protein. Neochromes were once thought to be unique to ferns, and were hypothesized to a play important role in facilitating ferns’ recent radiation in low-light environments.
By sieving through transcriptomic and genomic data, we recently discovered novel neochrome homologs in hornworts (a bryophyte lineage), and demonstrated that ferns acquired neochrome from hornworts via horizontal gene transfer (Li et al. 2014 PNAS). This work has important implications for the significance of horizontal gene transfer among eukaryotes, and was widely publicized in the media. In addition, we reconstructed the evolutionary histories of phytochromes and phototropins across land plants (Li et al. 2015 Frontiers in Plant Science; Li et al. 2015 Nature Communications), and we are building upon such framework to interpret what we know about Arabidopsis photobiology within a broader evolutionary context.