Third-codon transversion rate-based Nymphaea basal angiosperm phylogeny -- concordance with developmental evidence

Xiaohan Yang,(Max) Zong-Ming Cheng,Gerald Tuskan,Timothy Tschaplinski

doi:10.1038/npre.2007.320.1

Xiaohan Yang, (Max) Zong-Ming Cheng + Show 2 more

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https://doi.org/10.1038/npre.2007.320.1

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Abstract

AbstractFlowering plants (angiosperms) appeared on Earth rather suddenly approximately 130 million years ago and underwent a massive expansion in the subsequent 10-12 million years. Current molecular phylogenies have predominantly identified Amborella, followed by Nymphaea (water lilies) or Amborella plus Nymphaea, in the ANITA clade (Amborella, Nymphaeales, Illiciaceae, Trimeniaceae and Austrobaileyaceae) as the earliest angiosperm. However, developmental studies suggest that the earliest angiosperm had a 4-cell/4-nucleus female gametophyte and a diploid endosperm represented by Nymphaea, suggesting that Amborella, having an 8-cell/9-nucleus female gametophyte and a triploid endosperm, cannot be representative of the basal angiosperm. This evolution-development discordance is possibly caused by erroneous inference based on phylogenetic signals with low neutrality and/or high saturation. Here we show that the 3rd codon transversion (P3Tv), with high neutrality and low saturation, is a robust high-resolution phylogenetic signal for such divergences and that the P3Tv-based land plant phylogeny cautiously identifies Nymphaea, followed by Amborella, as the most basal among the angiosperm species examined in this study. This P3Tv-based phylogeny contributes insights to the origin of angiosperms with concordance to fossil and stomata development evidence.

Highlights

Flowering plants appeared on Earth approximately 130 million years ago and subsequently experienced a massive expansion over the 10-12 mya, resulting in much of the today’s flora (De Bodt, Maere, and Van de Peer 2005)
Plant evolutionary biologists have long attempted to reconstruct angiosperm evolutionary history in an effort to determine the root of angiosperms
Uncorrected pairwise sequence divergence (p-distance) and Kimura-corrected distance (Kimura 1980) were calculated using MBEToolbox (Cai et al 2005), for transitions (Ts), transversions (Tv), or Ts plus Tv at the 3rd-codon positions of the whole chloroplast genome coding sequences of 36 land plant taxa compiled by Qiu et al (Qiu et al 2006)

Summary

Introduction

Flowering plants (angiosperms) appeared on Earth approximately 130 million years (mya) ago and subsequently experienced a massive expansion over the 10-12 mya, resulting in much of the today’s flora (De Bodt, Maere, and Van de Peer 2005). This phenomenon was described by Darwin in 1879 as an “abominable mystery” (Darwin 1903). Developmental biologists have studied two key developmental aspects in the ANITA clade, i.e., the structure of female gametophyte and formation of embryo nourishing tissue (endosperm), to help clarify the origin of the extant angiosperms (Williams and Friedman 2002; Friedman and Williams 2003; Friedman and Williams 2004; Friedman 2006). All ANITA members except Amborella have a 4-cell/4-nucleus female gametophyte with one of the double fertilization events yielding a biparental diploid endosperm (Williams and Friedman 2002; Friedman and Williams 2003; Friedman and Williams 2004), whereas the rest of angiosperm species have an 8-cell/9-nucleus (Amborella) (Friedman 2006) or a 7-cell/8-nucleus (all non-ANITA angiosperms) female gametophyte, with one of the double fertilization events yielding a biparental triploid endosperm (Friedman and Williams 2003; 2004)

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