Genes for seeds arose early in the evolution of plants, ferns reveal | Science

The appearance of seed-producing plants more than 300 million years ago was an evolutionary watershed, opening up new environments for plants and eventually leading to the flowering plants that decorate our world and provide much of our food. But it was a smaller jump than newly published DNA sequences seem to suggest.

The genomes of three species of fern and cycad, one of the oldest species of seed plants, show that the genes key to seed creation are the same as those in the sporulation mechanism of ferns, which appeared tens of millions of years ago. They apparently existed in a common ancestor, but were involved in different reproductive functions when plants diverged.

The fern and cycad genomes, published in a series of papers over the past few months, “fill a gap in gene flow during plant evolution,” says Shu-Nong Bai, a plant developmental biologist emeritus at Peking University who helped sequence a member of the maidenhair fern genus. “Evolutionary innovations [can] originate from alternative uses of existing genes or networks rather than new genes.” Genomes also teach a second startling lesson: plants did not acquire some of their genes through mutation and selection, but directly from fungi or other microbes through a controversial process known as horizontal gene transfer.

Because of the daunting size of most fern genomes and the focus on crops such as rice, wheat, and maize, most of the more than 800 sequenced plant genomes come from seed plants. So far, only two have been from ferns — with extremely small genomes. As a result, “we only got a small snapshot of plant evolution,” says Blaine Marchant, a plant evolutionary geneticist at Stanford University.

Thanks to advances in sequencing long stretches of DNA and lower costs, his team and three other groups are now targeting ferns with more typical, large genomes, as well as a species of cycad, a non-flowering plant with bare seeds like pines and other conifers. “It’s great to finally see more diverse plant genomes sequenced,” says Jennifer Weiskever, an evolutionary biologist at Purdue University.

Fern genomes, each containing about 30,000 genes, reveal a set of genes previously associated with flowering plants that evolved more than 200 million years later. For example, Marchant and his colleagues reported on September 1 in The nature of plants that water fern Richard’s Ceratopterishas 10 members of a gene family known to control flowering time, seed germination and flower shape in small flowering plants, arabidopsis. Their role in ferns is unclear, but seven of these genes are active in the leaf where spores are produced, suggesting that they play a role in fern reproduction as well as in seed plants.

Jianbin Yan, a plant physiologist at the Institute of Agricultural Genomics of the Chinese Academy of Agricultural Sciences, and his colleagues found similar parallels in maidenhair fern, Adiantum hair-spring. Its DNA contains genes for transcription factors called EMS1 and TPD1, ​​proteins that in corn and other seed plants regulate genes involved in pollen development, Yan’s team reported in the same issue of the journal. The nature of plants. These pollen gene controllers are active in the maiden hair sporangia, the tissue where the spores develop.

Genes found in the fertile fronds of ferns, where spores are formed, have counterparts in seeds and pollen. DAVID RANDALL

The fern’s genome also contains three genes that regulate seed development in flowering plants, adds Hongzhi Kong, a plant evolutionary biologist at the Institute of Botany, Chinese Academy of Sciences. Yang says that ferns are “evolutionarily key to a comprehensive understanding of the origin and diversification of seeds.” The cycad genome contains similar networks, suggesting that they were active in the earliest seed plants, said Shouzhou Zhang, a botanist at the Fairy Lake Botanical Garden in Shenzhen who led its sequencing.

The new genomes shed light on one reason such ideas have been slow to arrive: Ferns are notoriously “known for having giant genomes,” says Fai-Wei Li, a plant evolutionary biologist at Cornell University. The researchers hypothesized that the size of the genome is due to a process called whole-genome duplication, in which the amount of an organism’s DNA doubles during reproduction. But “we’re not seeing the genome duplication that we thought we did,” says Paul Wolff, a plant geneticist at the University of Alabama, Huntsville. Instead, ferns and cycads got the bulk of their DNA through the accumulation of mobile DNA—transposons and other genetic elements that infect genomes and multiply, or repetitive, short sequences of DNA that are copied over and over again.

The four new genomes also change views on whether plants experience horizontal gene transfer. Microbes are known to constantly change genes to help them adapt to new conditions, but multicellular organisms seem to have borrowed genes only rarely. However, the genomes of ferns and cycads contain a surprising number of genes from bacteria and fungi. “It’s great that we’re seeing genes of bacterial and fungal origin in vascular plants,” says Kong.

For example, the sequenced cycad has four copies of the fungal gene for cytotoxin, a protein that can punch holes in foreign cells, and ceratopteris the genome contains 36 copies of another bacterial cytotoxin gene. These acquired genes could strengthen the new hosts’ defenses against pathogens or herbivores.

Veronica Di Stilio, a botanist at the University of Washington in Seattle, expects more surprises from the recently released genomes. “Having reference genomes representing each of the major plant lineages opens up so many possibilities,” she says. “Genomes are tools, the tip of the iceberg.”

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