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

First author: Rebecca A. Povilus; Affiliations: Harvard University (哈佛大学): Cambridge, USA

Corresponding author: William E. Friedman

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.

超过2.25亿年，所有的种子植物都是木本林木、灌木或藤蔓。在1.4亿年前被子植物起源后不久，睡莲目（Nymphaeales）植物丢失了能够产生次生木质部和韧皮部的分生组织细胞，即维管形成层，成为了第一批从木本植物祖先分化出来的支系之一。许多调控次生组织分化的基因和基因家族同样调控初生木质部和韧皮部的分化，其主要由顶端分生组织所产生的，并几乎在所有的种子植物中都保留了下来。本文中，作者测序并组装了一个侏儒卢旺达睡莲（Nymphaea thermarum）的基因组，睡莲是研究早期被子植物演化的模式物种，并与缺失形成层的单子叶植物（monocot）和形成层较少的莲属植物（Nelumbo）支系的植物基因组进行比较分析。该研究揭示了支系特异性的基因丢失和分化模式。睡莲属（Nymphaea）植物的基因组存在显著的HD-ZIP III转录因子家族收缩，尤其是丢失了REVOLUTA基因，REV基因在其它被子植物中影响形成层的活性。作者发现睡莲属和单子叶中形成层相关CLE信号多肽的拷贝显示出独特的替换，而该位点在其它植物中高度保守。莲属植物的形成层相关基因没有显示出明显的分化。维管形成层趋同丢失的分化基因组特征表明就算是多效基因也存在与性状丢失独立事件相关的独特分化模式。本文的研究结果为植物的草本性演化提供了新的视野，该特征是被子植物早期演化相关的关键生物创新之一。

通讯：William E. Friedman  (https://oeb.harvard.edu/people/william-friedman)

研究方向：开花植物的起源与随后的多样化，尤其是双受精和胚乳建立。

doi: https://doi.org/10.1073/pnas.1922873117

Journal: PNAS

Published date: March 31, 2020

p.s. 相关研究链接：

Nature：睡莲基因组

Nature Plants：睡莲目芡实与金鱼藻目金鱼藻基因组揭示早期被子植物演化