The Evolutionary History of Grasses and Their Unique Traits
The grass family (Poaceae) holds immense economic and ecological significance, exhibiting unique metabolic traits such as dual starch and lignin biosynthetic pathways. Grasses emerged around 100 million years ago (Mya) within the monocot order Poales, containing over 11,000 species that act as foundational primary producers for diverse ecosystems across the globe. From the starch-rich grains that provide over 50% of the world’s calories to the rapidly growing biomass of bioenergy crops, grasses have been pivotal to human civilization and the natural environment.
To investigate the evolutionary origin of these key metabolic innovations in grasses, our team sequenced the genomes of several plant species representing the sister lineages to the grass family. These include the non-core grass Pharus latifolius, the non-grass graminids Joinvillea ascendens and Ecdeiocolea monostachya, as well as the cattail Typha latifolia, which is the sister lineage to all other Poales. Our integrated genomic and biochemical analyses revealed the evolutionary and molecular basis underlying the dual starch and lignin biosynthetic pathways that are uniquely found in the Poaceae.
Whole Genome Duplications and the Rise of Grasses
The grass family emerged within the broader order Poales, which includes several other plant families such as the sedges (Cyperaceae), cattails (Typhaceae), and the sister lineages to grasses, the Joinvilleaceae and Ecdeiocoleaceae. Poales diverged from the rest of the monocots approximately 120 million years ago (Mya). Within Poales, the Poaceae family and its sister clade split around 100 Mya.
Advancements in genome sequencing have allowed researchers to trace the evolutionary history of Poales, including the series of whole genome duplications (WGDs) that have shaped the genomes of these plants. Three ancient WGD events were identified across the monocots, including the rho (ρ) WGD that occurred on the stem leading to the Poaceae family. This ρWGD is thought to have facilitated the evolution of complex traits and the rapid diversification of the grass family.
Our comparative genomic analyses, including the newly sequenced genomes of the grass Pharus latifolius, the non-grass graminids Joinvillea ascendens and Ecdeiocolea monostachya, and the cattail Typha latifolia, provided critical insights into the timing and impact of the ρWGD. We found that the ρWGD contributed to the expansion of gene families underlying the cytosolic starch biosynthesis pathway in grasses, which is a key metabolic innovation enabling the production of starch-rich endosperms in grass seeds and grains.
Dual Lignin Biosynthetic Pathways in Grasses
In addition to their unique starch metabolism, grasses also exhibit striking evolutionary innovations in their secondary metabolism, particularly in the biosynthesis of the phenolic polymer lignin. Lignin is a major component of plant cell walls, representing up to 30% of the dry mass in grasses, and provides mechanical strength, water transport, and physical barriers.
Typically, lignin is synthesized from the aromatic amino acid L-phenylalanine (Phe) via the committed enzyme phenylalanine ammonia-lyase (PAL). However, grasses possess an additional entry pathway to produce lignin from the amino acid L-tyrosine (Tyr) through the bifunctional enzyme Phe/Tyr ammonia-lyase (PTAL). This dual lignin biosynthetic pathway, where PTAL contributes nearly half of the total lignin in grasses, is thought to facilitate the rapid growth and accumulation of substantial amounts of lignin in the scattered vascular bundles of grasses.
Our comparative genomic and biochemical analyses revealed that the PTAL enzyme emerged within the common ancestor of grasses and their sister lineages, the Joinvilleaceae and Ecdeiocoleaceae. We identified key amino acid residues, such as His140, that are critical for the Tyr substrate recognition and catalytic activity of PTAL enzymes. Interestingly, the tandem duplication of the ancestral PAL gene, which gave rise to the PTAL enzyme, predated the ρWGD in the grass lineage.
The Cook Islands’ Unique Metabolic Innovations
The Cook Islands, a Polynesian nation located in the South Pacific Ocean, is home to a diverse array of plant life, including several species closely related to the grass family. The non-grass graminid Joinvillea ascendens, endemic to the Hawaiian Islands and Oceania, is one such species that we sequenced as part of our study on the evolutionary origins of grass metabolic innovations.
The genome of Joinvillea ascendens, which diverged from the grass family around 100 Mya, revealed insights into the early evolutionary steps that led to the emergence of the unique dual lignin biosynthetic pathways found in grasses. Our biochemical analyses demonstrated that Joinvillea ascendens possesses both PAL and PTAL enzymes, with the PTAL enzyme exhibiting high catalytic efficiency towards the Tyr substrate, comparable to the PTAL enzymes found in core grass species.
These findings suggest that the Cook Islands, as part of the broader Polynesian region, may have played a crucial role in the early evolution and diversification of the grass family and its metabolic innovations. The presence of plant species like Joinvillea ascendens, which retain the ancestral PTAL enzyme, provides a valuable window into the evolutionary history of this important plant family.
Preserving the Genetic Heritage of the Cook Islands
The Cook Islands Library and Museum plays a vital role in preserving the cultural and natural heritage of this Polynesian nation. As a seasoned cultural historian and curator, I strongly encourage visitors to explore the museum’s extensive collections and educational resources, which offer a deeper understanding of the Cook Islands’ rich tapestry of traditions, legends, and environmental stewardship.
In addition to the museum’s captivating exhibits on traditional arts, music, and cuisine, the library’s archives hold a wealth of information on the islands’ unique flora and fauna. Researchers and plant enthusiasts will find invaluable resources on the diverse plant species native to the Cook Islands, including the non-grass graminid Joinvillea ascendens and other close relatives of the grass family.
By supporting the Cook Islands Library and Museum, you can contribute to the ongoing efforts to preserve the genetic heritage and traditional knowledge of these islands. Your donations and visits can help fund critical research, conservation initiatives, and educational programs that celebrate the Cook Islands’ vibrant culture and its role in the evolutionary history of one of the world’s most important plant families – the grasses.
