Origin and genetic nature of polyploidy in paleoendemic coast redwood (Sequoia sempervirens(D. Don) Endl.)

Abstract

It is not known when the polyploid coast redwood (Sequoia sempervirens) evolved from its diploid ancestors, and what is its type of polyploidy. Whether close relatives of Sequoia, giant sequoia (Sequoiadendron giganteum) and dawn redwood (Metasequoia glyptostroboides), have possibly contributed to the ancestry of hexaploid of Sequoia remains an open question. The nature of hexaploidy in Sequoia has baffled biologists for more than a century. Based on the chromosome configurations in Sequoia, G. Ledyard Stebbins was the first geneticists who postulated in 1948 that Sequoia is an autoallohexaploid (AAAABB), and an ancient species of Metasequoia might have been one of the putative ancestors of Sequoia. After its chromosome number (2n=6x=66) was confirmed in hexaploid Sequoia, the type of polyploidy in Sequoia has been further investigated for the past 70 years by a number of investigators, using cytogenetic and genetic data. Although an autoallohexaploid (AAAABB) origin of Sequoia has remained one of the dominant hypotheses until recently, an alternative hypothesis, amongst other possible origins, was also put forth by Ahuja and Neale (2002), that Sequoia may be partially diploidized autohexaploid (AAAAAA), derived from some ancestral species of Sequoia, thus carrying a single ancestral genome. Cytogenetic, molecular genetics, and genome sequence data now support the hypothesis that Sequoia originated as an autohexaploid.

The Metasequoia genome and evolutionary relationships among redwoods

“…In addition to this hypothesis, our analysis suggests that dramatic genome reorganization during diploidization may result in the accumulation of deleterious mutations, and only a limited number of gymnosperm species can survive the genome shock. As reported previously, chromosomes in S. sempervirens meiotic cells are mostly in a bivalent state, but a few are in a multivalent state ( Ahuja and Neale, 2002 ). It has been proposed that S. sempervirens may be a complex species with different types of hexaploids and distinct genotypes ( Ahuja and Neale, 2002 ).…”

“…Our phylogenetic analyses of single-copy genes using three independent software programs (QuIBL, MSCquartets, and PhyloNet) also indicated that ILS rather than hybridization led to the inconsistent phylogenies ( Figure 3 ). The three extant redwood species exhibit both conserved and variant morphological and embryological characters ( Ahuja and Neale, 2002 ). The lineage-specific mutations and morphologies could have been caused by the independent evolutionary trajectories of the three species.…”

“…On the basis of chromosome configurations, Stebbins suggested that S. sempervirens might be an autoallopolyploid produced by hybridization between the ancient Metasequoia and some probably extinct taxodiaceous plants ( Stebbins, 1948 ). Seven models for the formation of hexaploid S. sempervirens have been proposed through analysis of fossil history, comparative morphology, karyotype analysis, and other data ( Ahuja and Neale, 2002 ). The hybridization process could be involved in formation of an autoallohexaploid (AABBBB or AAAABB), segmental allohexaploid (A1A1A1A1A2A2, A1A1A2A2A2A2, or A1A1A2A2A3A3), or a allohexaploid (AABBCC) ( Ahuja and Neale, 2002 ).…”

“…Seven models for the formation of hexaploid S. sempervirens have been proposed through analysis of fossil history, comparative morphology, karyotype analysis, and other data ( Ahuja and Neale, 2002 ). The hybridization process could be involved in formation of an autoallohexaploid (AABBBB or AAAABB), segmental allohexaploid (A1A1A1A1A2A2, A1A1A2A2A2A2, or A1A1A2A2A3A3), or a allohexaploid (AABBCC) ( Ahuja and Neale, 2002 ). Although the distributions of the three modern redwood species are distinct, fossil data suggest that they overlapped across the northern hemisphere from the Cretaceous period (∼145 Mya) ( Stockey et al., 2001 ).…”

“…proposed that S. sempervirens is most likely an autopolyploid ( Scott et al., 2016 ). Analysis of the S. sempervirens genome also indicated that S. sempervirens is a partially diploidized autohexaploid ( Neale et al., 2021 ; Ahuja, 2022 ). The genome sequence of M. glyptostroboides and comparative analysis with the genomes of S. giganteum and S. sempervirens ( Scott et al., 2020 ; Neale et al., 2021 ) will provide more resources for resolving questions about redwood evolution.…”