Chapter Eight - Aberration or Analogy? The Atypical Plastomes of Geraniaceae

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Abstract

A number of plant groups have been proposed as ideal systems to explore plastid inheritance, plastome evolution and plastome-nuclear genome coevolution. Quick generation times and a compact nuclear genome in Arabidopsis thaliana, the relative ease of plastid isolation from Spinacia oleracea and the tractability of plastid transformation in Nicotiana tabacum are all desirable attributes in a model system; however, these and most other groups all lack novelty in terms of plastome structure and nucleotide sequence evolution. Contemporary sequencing and assembly technologies have facilitated analyses of atypical plastomes and, as predicted by early investigations, Geraniaceae plastomes have experienced unprecedented rearrangements relative to the canonical structure and exhibit remarkably high rates of synonymous and nonsynonymous nucleotide substitutions. While not the only lineage with unusual plastome features, likely no other group represents the array of aberrant phenomena recorded for the family. In this chapter, Geraniaceae plastomes will be discussed and, where possible, compared with other taxa.

Introduction

Plastid genomes (plastomes) have been the subject of study since the recognition of their existence in plant and algal cells. Today nearly 2000 seed plant plastomes have been sequenced and analysed revealing genome-sized units (unit-genome) with highly conserved structure and gene content and limited variation in evolutionary rates. Typical angiosperm plastomes are maternally inherited and comprise many copies of the unit-genome, each containing a large inverted repeat (IR), a large and small single copy region (LSC and SSC, respectively) and approximately 120–130 genes mostly encoding ribosomal RNAs, transfer RNAs and proteins integral to plastid gene expression and photosynthesis. The genes are densely arrayed on both strands of plastome DNA, which typically has very low repetitive content. Variation in the order of genes is uncommon and more than half of the coding sequences are transcribed as polycistronic pre-mRNAs (Ruhlman & Jansen, 2014). Although the vast majority of seed plant plastomes conform to this description, there are several lineages that have experienced acceleration in nucleotide substitution rates and/or structural changes, including inversion, gene and intron loss, IR loss and accumulation of repetitive DNA (Jansen & Ruhlman, 2012).

Long before the genomic age and the advent of next-generation sequencing gave unprecedented access to plastome sequences, Geraniaceae were garnering attention. At the turn of the last century, Baur (1909) was exploring non-Mendelian inheritance patterns that he observed in the progeny of crosses between different Pelargonium zonale cultivars. Plastid inheritance is biparental in Pelargonium therefore hybrid zygotes can contain either maternal or paternal plastids or a mixture of both parental plastid types (Birky, 1995). Hybrid variegation can arise from disharmony between the hybrid nucleus and the plastome of one parent and is observed where both parents contribute plastids to the progeny, as in Pelargonium (Metzlaf, Pohlheim, Börner, & Hagemann, 1982; Metzlaff, Borner, & Hagemann, 1981; Weihe, Apitz, Pohlheim, Salinas-Hartwig, & Börner, 2009). Because plastid development and function is dependent on the nuclear genome, plastids bearing an incompatible plastome fail to develop in the hybrid, giving rise to white or yellow sectors on green leaves (Kirk & Tilney-Bassett, 1967).

Variegated congeneric hybrids, or so-called chimeras, of Pelargonium and Geranium were studied through the 1920s and 1930s (Hagemann, 2010), and among a very few other taxa were the workhorses of the evolving theories of organelle inheritance and extranuclear genetics. That trend continued through the 20th century and new techniques to examine plastid DNA and its inheritance were employed with Pelargonium. Southern blotting of digested plastid DNA revealed variation in the EcoRI fragments among P. zonale hybrids and found that the parental plastome genotypes (plasmotype) could be identified in the progeny using this technique (Metzlaff et al., 1981), providing a molecular link to the variegated phenotypes examined by Baur. Employing similar approaches, plastomes from four Geraniaceae genera were examined including P. × hortorum (Palmer, Nugent, & Herbon, 1987), Monsonia (formerly Sarcocolon), Geranium and Erodium (Palmer, 1991). The results suggested that an entire suite of plastome anomalies were present within the family.

Technology has permitted the sequencing and assembly of genomes and Geraniaceae plastomes are no exception. While the tantalizing results of early Southern analyses hinted at the unusual, contemporary methods have uncovered some of the most bizarre plastomes among seed plants. Here, the unusual features of Geraniaceae plastomes will be discussed and, where possible, compared with other taxa. Many of the changes in the family may be found in other lineages (Table 1, a, b, c, d); however, it appears likely that no other group of plants represents the range of plastome variation seen in Geraniaceae.

Section snippets

The Great and the Small

Among photosynthetic angiosperms Geraniaceae plastomes occupy extremes with regard to size, with a collection of phenomena that have inflated and diminutized them. As is the case in many groups, substantial changes in overall nucleotide content involve expansion and contraction of the IR. Plastomes have also been expanded through seemingly IR-independent repeat accumulation in the family and elsewhere. Although rare, incorporation of extraplastomic DNA (native mitochondrial) has influenced

Change or Stay the Same

Recombination between IR copies within a unit-genome, or between any part of the unit-genome and another copy in the highly iterative plastome is thought to maintain uniformity in typical angiosperm plastomes. When a mutation arises, it does so at a single locus. Persistence of the mutation or a return to the original state depends on recombination between individual copies (or alleles) of the locus. Given the large number of unit-genome copies that are available to template copy correction, it

Keeping Up With the Rate Race: Acceleration and Coevolution

Geraniaceae plastomes have experienced structural changes that have enlarged and diminished them including IR boundary changes and IR loss, accumulation of repeated sequence and sequence loss (Weng et al., 2014). Because the plastid unit-genome is iterative, gene conversion, one of the mechanisms responsible for maintaining plastome uniformity, can also participate in elevating evolutionary rates or driving mutations to fixation. Repeat content has been linked to rate acceleration in

Staying in Sync: Hybrid Harmony or Dissonance

Hypotheses have suggested that a major impetus for the ongoing transfer of genes formerly encoded in the endosymbiont to the host nucleus could be related to the different mutation rates between compartments (Brandvain & Wade, 2009), although in typical angiosperms plastome rates are approximately one-fifth that of the nucleus (Drouin et al., 2008). Perhaps the ameliorating effect of sexual recombination on deleterious mutations has driven transfer of organelle genes to the nuclear genome. In

Aberration or Analogy?

Apart from the incorporation of foreign DNA by intracellular or horizontal transfer virtually every type of plastome abnormality has been detected in Geraniaceae. Although not necessarily analogical, there are other groups that display one or several of the phenomena exhibited in Geraniaceae plastomes (Table 1). Where there are similar outcomes in terms of the nucleotide substitution rate acceleration or structural divergence, it is nonetheless difficult to postulate an overarching mechanism or

Acknowledgements

The authors gratefully acknowledge support from the National Science Foundation (IOS-1027259 to R.K.J. and T.A.R.) and from Vice President for Educational Affairs Abdulrahman O. Alyoubi at King Abdulaziz University, Jeddah, Saudi Arabia (to R.K.J.). We also thank the many students, graduates and undergraduates, over more than 10 years whose efforts and contributions made the Geraniaceae Genomes Project possible including Tim Chumley, Mary Guisinger, J. Chris Blazier, Mao-Lun Weng, Jin Zhang,

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