Water lily ( Nymphaea thermarum ) genome reveals variable genomic signatures of ancient vascular cambium losses

Abstract

For more than 225 million y, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of angiosperms ∼140 million y ago (MYA), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium, the meristematic population of cells that produces secondary xylem (wood) and phloem. Many of the genes and gene families that regulate differentiation of secondary tissues also regulate the differentiation of primary xylem and phloem, which are produced by apical meristems and retained in nearly all seed plants. Here, we sequenced and assembled a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compared it to genomes from other cambium-bearing and cambium-less lineages (e.g., monocots and Nelumbo). This revealed lineage-specific patterns of gene loss and divergence. Nymphaea is characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss of REVOLUTA, which influences cambial activity in other angiosperms. We also found the Nymphaea and monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids. Nelumbo displays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent loss of vascular cambium reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent events of trait loss. Our results shed light on the evolution of herbaceousness—one of the key biological innovations associated with the earliest phases of angiosperm evolution.

The Histone Acetyltransferase GCN5 and the Associated Coactivators ADA2: From Evolution of the SAGA Complex to the Biological Roles in Plants

“…In the first angiosperm and the most basal extant flowering plant genome of Amborella trichopoda [ 54 ] as well as in the nonwoody aquatic Nymphaea species [ 55 ], all the components of the SAGA complex were observed, some of them in duplication (e.g., ADA3, ADA1, and TAF12). Moving higher in the angiosperms, SGF73 subunit was not detected in the monocots and eudicots, suggesting that this gene was lost during plant evolution.…”

The Woody Planet: From Past Triumph to Manmade Decline

“…When gymnosperms, especially conifers, started to dominate our planet, they quickly left only epiphytic, aquatic or marginal niches for lycophytes and monilophytes [ 6 ]. Consequently, for more than 225 million years, the planet Earth was a true woody planet, since all seed plants were woody trees, shrubs or lianas [ 12 ]. Interestingly, the early history of angiosperms—the most diverse and dominant plant group today—also seemed to be woody [ 7 , 13 , 14 ].…”

“…Interestingly, there are five taxonomic lineages across angiosperms that are not only exclusively herbaceous but that have in fact completely lost the vascular cambium during their evolution: (1) the whole order Nymphaeales, the plants of the genera (2) Ceratophyllum and (3) Nelumbo , (4) the family Podostemaceae and (5) all monocots [ 12 ]. For the first four plant groups, the convergent loss of the vascular cambium appears to be associated with the transition to an aquatic habitat [ 14 ].…”

Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales) reveal dynamic expression of DNA and histone methylation modifiers

“…While this is related to the difficulty of working with the vast majority of species within these lineages (e.g., Amborella, Nymphaeales, Austrobaileyales, Chloranthales, Ceratophyllales, magnoliids, which are typically longlived trees, shrubs, lianas, or aquatic plants), a genetically and experimentally tractable species from within one of the most-early diverging lineages has been identified (Povilus 2015). Nymphaea thermarum (Nymphaeales) is a minute waterlily with a relatively short generation time and a draft genome assembly and annotation (Povilus 2020) -as such, it is poised to help illuminate questions about the evolution of flowering plant reproduction.…”