For ∼225 million y, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of flowering plants ∼140 million y ago, Nymphaeales (water lilies) became one of the first seed plant lineages to become herbaceous through loss of the meristematic cell population known as the vascular cambium.

We sequenced and assembled the draft genome of the water lily Nymphaea thermarum and compared it to genomes of other plants that have retained or lost the vascular cambium. By using both genome-wide and candidate-gene analysis, we found lineage-specific patterns of gene loss and divergence associated with cambium loss. Our results reveal divergent genomic signatures of convergent trait loss in a system characterized by complex gene-trait relationships.

 

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.

 

See https://www.pnas.org/content/117/15/8649

 

 

Figure 1: Vascular cambium evolution and stem vascular anatomy in flowering plants. (A) Abbreviated phylogenetic relationships of major clades of seed plants, with notes on diversity of growth habits found in each group. MYA, million years ago. (B) Growth habit of Nymphaea thermarum. (C) One individual of N. thermarum. Red line indicates in situ soil level. (Scale bar, 15 cm.) (D) Close-up of rhizome from C. Arrowhead, apical meristem; black line, living rhizome section; dashed line, dead rhizome section. (E) Stem vascular anatomy in clades of flowering plants. Cross-sections were taken from maturing (Medicago) or mature (ZeaNelumboNymphaea) stems. (Top Row) Micrographs (MedicagoZeaNymphaea) or drawings based on prepared slides (Nelumbo) of vascular bundles. (Scale bars, 20 μm.) (Middle Row) Vascular components labeled and color-coded. f (green), fibers; ph + pa (pink), phloem and vascular parenchyma; vc (yellow), vascular cambium; xy (blue), xylem. (Bottom Row) Whole stem sections. red, vascular bundles and tissue in cross-section; yellow, vascular cambium; black, vascular bundles that are part of a leaf or flower trace; gray, nonvascular tissue. (Scale bars, 0.5 mm.) Nelumbo panels adapted with permission from ref. 27.