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A novel approach to study the morphology and chemistry of pollen in a phylogenetic context, applied to the halophytic taxon Nitraria L.(Nitrariaceae).

ABSTRACT: Nitraria is a halophytic taxon (i.e., adapted to saline environments) that belongs to the plant family Nitrariaceae and is distributed from the Mediterranean, across Asia into the south-eastern tip of Australia. This taxon is thought to have originated in Asia during the Paleogene (66-23 Ma), alongside the proto-Paratethys epicontinental sea. The evolutionary history of Nitraria might hold important clues on the links between climatic and biotic evolution but limited taxonomic documentation of this taxon has thus far hindered this line of research. Here we investigate if the pollen morphology and the chemical composition of the pollen wall are informative of the evolutionary history of Nitraria and could explain if origination along the proto-Paratethys and dispersal to the Tibetan Plateau was simultaneous or a secondary process. To answer these questions, we applied a novel approach consisting of a combination of Fourier Transform Infrared spectroscopy (FTIR), to determine the chemical composition of the pollen wall, and pollen morphological analyses using Light Microscopy (LM) and Scanning Electron Microscopy (SEM). We analysed our data using ordinations (principal components analysis and non-metric multidimensional scaling), and directly mapped it on the Nitrariaceae phylogeny to produce a phylomorphospace and a phylochemospace. Our LM, SEM and FTIR analyses show clear morphological and chemical differences between the sister groups Peganum and Nitraria. Differences in the morphological and chemical characteristics of highland species (Nitraria schoberi, N. sphaerocarpa, N. sibirica and N. tangutorum) and lowland species (Nitraria billardierei and N. retusa) are very subtle, with phylogenetic history appearing to be a more important control on Nitraria pollen than local environmental conditions. Our approach shows a compelling consistency between the chemical and morphological characteristics of the eight studied Nitrariaceae species, and these traits are in agreement with the phylogenetic tree. Taken together, this demonstrates how novel methods for studying fossil pollen can facilitate the evolutionary investigation of living and extinct taxa, and the environments they represent.

SUBMITTER: Woutersen A

PROVIDER: S-EPMC6054868 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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A novel approach to study the morphology and chemistry of pollen in a phylogenetic context, applied to the halophytic taxon Nitraria L.(Nitrariaceae).

Woutersen Amber A Jardine Phillip E PE Bogotá-Angel Raul Giovanni RG Zhang Hong-Xiang HX Silvestro Daniele D Antonelli Alexandre A Gogna Elena E Erkens Roy H J RHJ Gosling William D WD Dupont-Nivet Guillaume G Hoorn Carina C

PeerJ 20180719

Nitraria is a halophytic taxon (i.e., adapted to saline environments) that belongs to the plant family Nitrariaceae and is distributed from the Mediterranean, across Asia into the south-eastern tip of Australia. This taxon is thought to have originated in Asia during the Paleogene (66-23 Ma), alongside the proto-Paratethys epicontinental sea. The evolutionary history of Nitraria might hold important clues on the links between climatic and biotic evolution but limited taxonomic docu ...[more]

PMID: 30038851

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Project description:Intragenomic polymorphism of ITS1 and ITS2 of nuclear ribosomal DNA sequences was analysed in 33 samples belonging to the Nitraria species N. schoberi, N. sibirica, and N. komarovii. The nucleotide variability of the ITS region was detected in the Nitraria species as single-nucleotide substitutions (mainly transitions) and single-nucleotide deletion. Information about the nucleotide variability of fragments is given for the first time by us. The ITS1-5.8S-ITS2 region contained 17 phylogenetically informative single-nucleotide polymorphisms. Eleven single-nucleotide substitutions (transitions, C/T) were detected in ITS1. The ITS2 spacer contained 273-274 bp and was more conservative. A total of 5 phylogenetically informative single-nucleotide polymorphisms (4 transitions: C/T, G/A, one transversion: G/C), one single-nucleotide deletion (T/-) were detected in ITS2. The average GC content was 61.5 %. The GC content was lower in N. sibirica (59.2 %) than in N. schoberi and N. komarovii (62.7 %). It has been shown that the shorter ITS2 is a suitable molecular marker separating these species, due to the low interspecific variability and simultaneous available intraspecific variability. Phylogenetic ML and BI trees constructed separately for the ITS1 and ITS2 spacers, as well as separately for the full-size ITS region and the ITS2 spacer, were congruent. The results obtained on the intraspecific differentiation of N. sibirica revealed two main ribotypes among the samples of this species: the main Siberian sibirica-ribotype and the main Kazakh sibiricaribotype. Geographical features of the distribution of N. sibirica ribotypes, as well as the presence of significant differences between the main Siberian and Kazakh sibirica-ribotypes (3 single-nucleotide substitutions) indicated significant inter-population differences and taxonomic heterogeneity of N. sibirica. Most likely, the processes of homogenization of nuclear ribosomal DNA of N. sibirica samples, the origin of which is associated with hybridization and speciation, are currently continuing.

Project description:The study of pollen morphology has historically allowed evolutionary biologists to assess phylogenetic relationships among Angiosperms, as well as to better understand the fossil record. During this process, pollen has mainly been studied by discretizing some of its main characteristics such as size, shape, and exine ornamentation. One large plant clade in which pollen has been used this way for phylogenetic inference and character mapping is the order Myrtales, composed by the small families Alzateaceae, Crypteroniaceae, and Penaeaceae (collectively the "CAP clade"), as well as the large families Combretaceae, Lythraceae, Melastomataceae, Myrtaceae, Onagraceae and Vochysiaceae. In this study, we present a novel way to study pollen evolution by using quantitative size and shape variables. We use morphometric and morphospace methods to evaluate pollen change in the order Myrtales using a time-calibrated, supermatrix phylogeny. We then test for conservatism, divergence, and morphological convergence of pollen and for correlation between the latitudinal gradient and pollen size and shape. To obtain an estimate of shape, Myrtales pollen images were extracted from the literature, and their outlines analyzed using elliptic Fourier methods. Shape and size variables were then analyzed in a phylogenetic framework under an Ornstein-Uhlenbeck process to test for shifts in size and shape during the evolutionary history of Myrtales. Few shifts in Myrtales pollen morphology were found which indicates morphological conservatism. Heterocolpate, small pollen is ancestral with largest pollen in Onagraceae. Convergent shifts in shape but not size occurred in Myrtaceae and Onagraceae and are correlated to shifts in latitude and biogeography. A quantitative approach was applied for the first time to examine pollen evolution across a large time scale. Using phylogenetic based morphometrics and an OU process, hypotheses of pollen size and shape were tested across Myrtales. Convergent pollen shifts and position in the latitudinal gradient support the selective role of harmomegathy, the mechanism by which pollen grains accommodate their volume in response to water loss.

Dataset Information

A novel approach to study the morphology and chemistry of pollen in a phylogenetic context, applied to the halophytic taxon Nitraria L.(Nitrariaceae).

Publications

A novel approach to study the morphology and chemistry of pollen in a phylogenetic context, applied to the halophytic taxon <i>Nitraria</i> L.(Nitrariaceae).

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