Reconstructing development of the earliest seed integuments raises a new hypothesis for the evolution of ancestral seed-bearing structures

Research output: Contribution to journalArticlepeer-review

Colleges, School and Institutes

Abstract

How plant seeds originated remains unresolved, in part due to disconnects between fossil intermediates and developmental genetics in extant species. The Carboniferous fossil Genomosperma is considered among the most primitive known seeds, with highly lobed integument and exposed nucellus. We have used this key fossil taxon to investigate the evolutionary origins of seed development. We examined sectioned Genomosperma specimens using modern digital 3D reconstruction techniques and established population-level measurements of Genomosperma ovules for quantitative analysis. Genomosperma ovules show significant variation in integumentary lobe fusion and curvature. Our analysis suggests that this variation represents a single species with significant variations in lobe number and fusion, reminiscent of floral development in extant species. We conclude that changes in lobe flexure occurred late in development, consistent with a previously hypothesized function in pollen guidance/retention. We also identify seeds of Genomosperma within cupules for the first time. The presence of a cupule adds evidence towards the plesiomorphy of cupules within seed plants. Together with the similarities identified between the Genomosperma lobed integument and floral organs, we propose that the cupule, integument and nucellus together developed in a shoot-like fashion, potentially ancestral to extant seed plant reproductive shoots.

Bibliographic note

Funding Information: This research is dedicated to the memory of Albert G. Long for his pioneering and lasting palaeobotany investigations that paved the way to our understanding of the earliest seed plants. We thank Sylvia Humphrey (Great North Museum, Hancock), Neil Clarke and Jeff Liston (Hunterian Museum, University of Glasgow) for specimen loans, Zoe Wickens for conducting preliminary investigations, David Long (Royal Botanic Gardens, Edinburgh) for providing literature, and Andrew R. Rees (Birmingham) and Alan Spencer (Imperial College, London) for help with Spiers. Richard Bateman, Nick Rowe, Gar Rothwell, Susana Magallon and an anonymous reviewer are thanked for reviewing the manuscript. This research was conducted as an undergraduate research project by LEM at the University of Birmingham; financial support was provided by the School of Geography, Earth and Environmental Sciences. ARGP is supported by a Royal Society University Research Fellowship. The authors declare no conflict of interest. Publisher Copyright: © 2020 The Authors New Phytologist ©2020 New Phytologist Foundation Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

Details

Original languageEnglish
Pages (from-to)1782-1794
Number of pages13
JournalNew Phytologist
Volume229
Issue number3
Early online date8 Jul 2020
Publication statusPublished - Feb 2021

Keywords

  • 3D reconstruction, cupule, evolution, gene networks, gymnosperm, integument, ovule, pteridosperm

ASJC Scopus subject areas