scholarly journals Degradation of key photosynthetic genes in the critically endangered semi-aquatic flowering plant Saniculiphyllum guangxiense (Saxifragaceae)

Author(s):  
Ryan A. Folk ◽  
Neeka Sewnath ◽  
Chun-Lei Xiang ◽  
Brandon T. Sinn ◽  
Robert P. Guralnick

AbstractBackgroundPlastid gene loss and pseudogenization has been widely documented in parasitic and mycoheterotrophic plants, which have relaxed selective constraints on photosynthetic function. More enigmatic are sporadic reports of degradation and loss of important photosynthesis genes in lineages thought to be fully photosynthetic. Here we report the complete plastid genome of Saniculiphyllum guangxiense, a critically endangered and phylogenetically isolated plant lineage, along with genomic evidence of reduced chloroplast function. We also report 22 additional plastid genomes representing the diversity of its containing clade Saxifragales, characterizing gene content and placing variation in a broader phylogenetic context.ResultsWe find that the plastid genome of Saniculiphyllum has experienced pseudogenization of five genes of the NDH complex (ndhA, ndhB, ndhD, ndhF, and ndhK), previously reported in flowering plants with an aquatic habit, as well as the more surprising pseudogenization of two genes more central to photosynthesis (ccsA and cemA), contrasting with strong phylogenetic conservatism of plastid gene content in all other sampled Saxifragales. These genes participate in photooxidative protection, cytochrome synthesis, and carbon uptake. Nuclear paralogs exist for all seven plastid pseudogenes, yet these are also unlikely to be functional.ConclusionsSaniculiphyllum appears to represent the greatest degree of plastid gene loss observed to date in any fully photosynthetic lineage, yet plastid genome length, structure, and substitution rate are within the variation previously reported for photosynthetic plants. These results highlight the increasingly appreciated dynamism of plastid genomes, otherwise highly conserved across a billion years of green plant evolution, in plants with highly specialized life history traits.

PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e7500 ◽  
Author(s):  
Mikhail I. Schelkunov ◽  
Maxim S. Nuraliev ◽  
Maria D. Logacheva

Although most plant species are photosynthetic, several hundred species have lost the ability to photosynthesize and instead obtain nutrients via various types of heterotrophic feeding. Their plastid genomes markedly differ from the plastid genomes of photosynthetic plants. In this work, we describe the sequenced plastid genome of the heterotrophic plant Rhopalocnemis phalloides, which belongs to the family Balanophoraceae and feeds by parasitizing other plants. The genome is highly reduced (18,622 base pairs vs. approximately 150 kbp in autotrophic plants) and possesses an extraordinarily high AT content, 86.8%, which is inferior only to AT contents of plastid genomes of Balanophora, a genus from the same family. The gene content of this genome is quite typical of heterotrophic plants, with all of the genes related to photosynthesis having been lost. The remaining genes are notably distorted by a high mutation rate and the aforementioned AT content. The high AT content has led to sequence convergence between some of the remaining genes and their homologs from AT-rich plastid genomes of protists. Overall, the plastid genome of R. phalloides is one of the most unusual plastid genomes known.


2018 ◽  
Author(s):  
Mikhail I. Schelkunov ◽  
Maxim S. Nuraliev ◽  
Maria D. Logacheva

AbstractAlthough most plant species are photosynthetic, several hundred species have lost the ability to photosynthesize and instead obtain nutrients via various types of heterotrophic feeding. Their genomes, especially plastid genomes, markedly differ from the genomes of photosynthetic plants. In this work, we describe the sequenced plastid genome of the heterotrophic plant Rhopalocnemis phalloides, which belongs to the family Balanophoraceae and feeds by parasitizing on other plants. The genome is highly reduced (18 622 base pairs versus approximately 150 kilobase pairs in autotrophic plants) and possesses an outstanding AT content, 86.8%, the highest of all sequenced plant plastid genomes. The gene content of this genome is quite typical of heterotrophic plants, with all of the genes related to photosynthesis having been lost. The remaining genes are notably distorted by a high mutation rate and the aforementioned AT content. The high AT content has led to sequence convergence between some of the remaining genes and their homologues from AT-rich plastid genomes of protists. Overall, the plastid genome of R. phalloides is one of the most unusual plastid genomes known.


Plants ◽  
2020 ◽  
Vol 9 (3) ◽  
pp. 306 ◽  
Author(s):  
Matthias Jost ◽  
Julia Naumann ◽  
Nicolás Rocamundi ◽  
Andrea A. Cocucci ◽  
Stefan Wanke

Plastomes of parasitic and mycoheterotrophic plants show different degrees of reduction depending on the plants’ level of heterotrophy and host dependence in comparison to photoautotrophic sister species, and the amount of time since heterotrophic dependence was established. In all but the most recent heterotrophic lineages, this reduction involves substantial decrease in genome size and gene content and sometimes alterations of genome structure. Here, we present the first plastid genome of the holoparasitic genus Prosopanche, which shows clear signs of functionality. The plastome of Prosopanche americana has a length of 28,191 bp and contains only 24 unique genes, i.e., 14 ribosomal protein genes, four ribosomal RNA genes, five genes coding for tRNAs and three genes with other or unknown function (accD, ycf1, ycf2). The inverted repeat has been lost. Despite the split of Prosopanche and Hydnora about 54 MYA ago, the level of genome reduction is strikingly congruent between the two holoparasites although highly dissimilar nucleotide sequences are observed. Our results lead to two possible evolutionary scenarios that will be tested in the future with a larger sampling: 1) a Hydnoraceae plastome, similar to those of Hydnora and Prosopanche today, existed already in the most recent common ancestor and has not changed much with respect to gene content and structure, or 2) the genome similarities we observe today are the result of two independent evolutionary trajectories leading to almost the same endpoint. The first hypothesis would be most parsimonious whereas the second would point to taxon dependent essential gene sets for plants released from photosynthetic constraints.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9157
Author(s):  
Zhanghai Li ◽  
Xiao Ma ◽  
Yi Wen ◽  
Sisi Chen ◽  
Yan Jiang ◽  
...  

Mycoheterotrophic plants are highly specialized species able to acquire organic carbon from symbiotic fungi, with relaxed dependence on photosynthesis for carbon fixation. The relaxation of the functional constraint of photosynthesis and thereby the relaxed selective pressure on functional photosynthetic genes usually lead to substantial gene loss and a highly degraded plastid genome in heterotrophs. In this study, we sequenced and analyzed the plastome of the eudicot Exacum paucisquama, providing the first plastid genome of a mycoheterotroph in the family Gentianaceae to date. The E. paucisquama plastome was 44,028 bp in length, which is much smaller than the plastomes of autotrophic eudicots. Although the E. paucisquama plastome had a quadripartite structure, a distinct boundary shift was observed in comparison with the plastomes of other eudicots. We detected extensive gene loss and only 21 putative functional genes (15 protein-coding genes, four rRNA genes and two tRNA genes). Our results provide valuable information for comparative evolutionary analyses of plastomes of heterotrophic species belonging to different phylogenetic groups.


2014 ◽  
Author(s):  
Gavin Douglas ◽  
Gesseca Gos ◽  
Kim Steige ◽  
Adriana Salcedo ◽  
Karl Holm ◽  
...  

Whole genome duplication events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole genome data provide strong support for recent hybrid origins of the tetraploid species within the last 100-300,000 years from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide, due to the combined effects of demography, selfing and genome redundancy from whole genome duplication. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that non-functionalization can receive a 'head start' through a legacy of deleterious variants and differential expression originating in parental diploid populations.


2015 ◽  
Vol 112 (9) ◽  
pp. 2806-2811 ◽  
Author(s):  
Gavin M. Douglas ◽  
Gesseca Gos ◽  
Kim A. Steige ◽  
Adriana Salcedo ◽  
Karl Holm ◽  
...  

Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000–300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that nonfunctionalization can receive a “head start” through a legacy of deleterious variants and differential expression originating in parental diploid populations.


2019 ◽  
Author(s):  
Rebecca A. Povilus ◽  
Jeffery M. DaCosta ◽  
Christopher Grassa ◽  
Prasad R. V. Satyaki ◽  
Morgan Moeglein ◽  
...  

AbstractFor more than 225 million years, all seed plants were woody trees, shrubs, or vines (1–4). Shortly after the origin of angiosperms ~135 million years ago (MYA) (5), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium (6), 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 (7–9), which are produced by apical meristems and retained in nearly all seed plants. Here we sequence and assemble a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compare it to genomes from other cambium-bearing and cambium-less lineages (like monocots and Nelumbo). This reveals 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 find 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 vascular cambium loss reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent trait loss events. Our results shed light on the evolution of herbaceousness – one of the key biological innovations associated with the earliest phases of angiosperm evolution.Significance StatementFor ~225 million years, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of flowering plants ~135 million years 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 sequence and assemble the draft genome of the water lily Nymphaea thermarum, and compare it to genomes of other plants that have retained or lost the vascular cambium. By using both genome-wide and candidate-gene analysis, we find lineage-specific patterns of gene loss and divergence associated with cambium loss. Our reveal divergent genomic signatures of convergent trait loss in a system characterized by complex gene-trait relationships.


2020 ◽  
Vol 28 (1) ◽  
pp. 24-28
Author(s):  
Mahnaz Heidari Rikan ◽  
Farrokh Ghahremaninejad ◽  
Mostafa Assadi

Silene lulakabadensis Heidari, F. Ghahrem. & Assadi is described as a new species from Zanjan Province, Iran. The new species is a dark green plant, perennial and woody at the base, that was collected on marl soil slopes at 2100 m. It is believed to be closely related to S. eriocalycina Boiss. from section Auriculatae (Boiss.) Schischk. but is a smaller plant, with much shorter internodes, and pinkish-white retuse to emarginate petals with very small or no scales. It is a very rare plant and its conservation status is assessed as Critically Endangered.


2014 ◽  
Vol 369 (1648) ◽  
pp. 20130348 ◽  
Author(s):  
Lena C. Hileman

A striking aspect of flowering plant (angiosperm) diversity is variation in flower symmetry. From an ancestral form of radial symmetry (polysymmetry, actinomorphy), multiple evolutionary transitions have contributed to instances of non-radial forms, including bilateral symmetry (monosymmetry, zygomorphy) and asymmetry. Advances in flowering plant molecular phylogenetic research and studies of character evolution as well as detailed flower developmental genetic studies in a few model species (e.g. Antirrhinum majus , snapdragon) have provided a foundation for deep insights into flower symmetry evolution. From phylogenetic studies, we have a better understanding of where during flowering plant diversification transitions from radial to bilateral flower symmetry (and back to radial symmetry) have occurred. From developmental studies, we know that a genetic programme largely dependent on the functional action of the CYCLOIDEA gene is necessary for differentiation along the snapdragon dorsoventral flower axis. Bringing these two lines of inquiry together has provided surprising insights into both the parallel recruitment of a CYC -dependent developmental programme during independent transitions to bilateral flower symmetry, and the modifications to this programme in transitions back to radial flower symmetry, during flowering plant evolution.


Sign in / Sign up

Export Citation Format

Share Document