Evolution of the rpoB-psbZ region in fern plastid genomes: notable structural rearrangements and highly variable intergenic spacers

Gao et al. BMC Plant Biology 2011, 11:64 http://www.biomedcentral.com/1471-2229/11/64 RESEARCH ARTICLE Open Access Evolution of the rpoB-psbZ region in fern plastid genomes: notable structural rearrangements and highly variable intergenic spacers Lei Gao1, Yuan Zhou1, Zhi-Wei Wang1, Ying-Juan Su2* and Ting Wang1* Abstract Background: The rpoB-psbZ (BZ) region of some fern plastid genomes (plastomes) has been noted to go through considerable genomic changes. Unraveling its evolutionary dynamics across all fern lineages will lead to clarify the fundamental process shaping fern plastome structure and organization. Results: A total of 24 fern BZ sequences were investigated with taxon sampling covering all the extant fern orders. We found that: (i) a tree fern Plagiogyria japonica contained a novel gene order that can be generated from either the ancestral Angiopteris type or the derived Adiantum type via a single inversion; (ii) the trnY-trnE intergenic spacer (IGS) of the filmy fern Vandenboschia radicans was expanded 3-fold due to the tandem 27-bp repeats which showed strong sequence similarity with the anticodon domain of trnY; (iii) the trnY-trnE IGSs of two horsetail ferns Equisetum ramosissimum and E. arvense underwent an unprecedented 5-kb long expansion, more than a quarter of which was consisted of a single type of direct repeats also relevant to the trnY anticodon domain; and (iv) ycf66 has independently lost at least four times in ferns. Conclusions: Our results provided fresh insights into the evolutionary process of fern BZ regions. The intermediate BZ gene order was not detected, supporting that the Adiantum type was generated by two inversions occurring in pairs. The occurrence of Vandenboschia 27-bp repeats represents the first evidence of partial tRNA gene duplication in fern plastomes. Repeats potentially forming a stem-loop structure play major roles in the expansion of the trnY-trnE IGS. Background In contrast to nuclear and mitochondrial genomes, plant plastid (chloroplast) genomes (plastomes) are generally conserved in genome size, gene content and gene order [1-3]. This high conservation makes the plastid genes and genomes quite amenable for sequencing and be widely used in evolutionary and phylogenetic studies. Nevertheless, comparative genomics studies demonstrate that the plastomes of several vascular plant lineages such as lycophytes (Selaginellaceae) [4,5], gymnosperms (e.g. Pinaceae [6-8], Cupressaceae [9], Welwitschiaceae [7,10], Gnetaceae and Ephedraceae [7]) and various eudicot angiosperm lineages (e.g. Geraniaceae [2,11], Campanulaceae [12,13] * Correspondence: ; 1 CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China 2 State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China Full list of author information is available at the end of the article and Fabaceae [14,15]), have experienced remarkable genomic changes including significant size variations, complex rearrangements as well as substantial gene losses. Many reports have shown that highly rearranged plastomes usually contain a large number of repetitive elements [2,11,12,16]. Furthermore, the distribution of the repeats also exhibits a tendency to flank the rearrangement endpoints, implying an association between the repeat and the rearrangement [2,9,11,12,16-18]. Recently, Maréchal and Brisson [19] specified that the suppression of recombination between repeats is of importance in the maintenance of plastome stability. Nevertheless, besides rearrangement endpoints, abundant repeats are also found in other regions of plastomes. For instance, extensive dispersed repeats have been found throughout the algae plastome of Chlamydomonas reinhardtii [20], and many direct repeats derived from partial duplication of their nearby trnY-GUA gene have been observed in Douglas-fir (Pseudotsuga menziesii) [21]. These findings highlight the structural and © 2011 Gao et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Gao et al. BMC Plant Biology 2011, 11:64 http://www.biomedcentral.com/1471-2229/11/64 functional significances of chloroplast DNA (cpDNA) repeats. In Chlamydomonas plastomes, it has been shown that small dispersed repeats can influence both transcript stability and translation efficiency [22] or even function in DNA repair [23]. Previous studies, particularly those on the complete plastome sequences, have well documented the characteristics and distribution of cpDNA repeats [2,9,11,12,16,20,24,25]. However, very few investigations deal with the implications of the secondary structure of cpDNA repetitive elements on their origin, proliferation and potential function [26]. Delineating the secondary structural features should greatly facilitate our understanding of plastome evolution. A number of comparative chloroplast genomic studies have uncovered structural mutations in fern (monilophyte) cpDNAs, including as many as 6 inversions and a few gene losses [24,27-32]. Specifically, one ~3.3 kb inversion (involving trnG-GCC to trnT-GGU) [27] and an inverted trnDGUC gene (D inversion) [24] have been detected across ferns relative to other land plants. According to gene orders, the fern plastomes can be classified into two main types. One comprises the plastomes of taxa diversifying before the separation of the Schizaeales, which share the ancestral gene order and has been assumed to undergo no major rearrangements [33]. By contrast, the other composes the plastomes of core leptosporangiates possessing the derived gene order [33]. This derived gene order is characteristic of highly rearranged inverted repeats (IRs) with the rRNA genes arranged in reverse order in comparison to all other plants [34]. The rearranged IRs and their adjacent section of large single copy (LSC) region are thought to be generated by two partially overlapping inversions spanning LSC and IR regions [35]. Wolf et al. [33] recently illustrated that the two putative inversions occurred in pairs on the branch leading to the common ancestor of schizaeoid and core leptosporangiate ferns. The next striking difference between the ancestral and derived gene order is occurred between the rpoB and psbZ (BZ) in LSC region (Figure 1a). BZ region is characterized with a high degree of variability. Each of the three key inversions shaping the ancestral gene order of ferns, i.e. the 30-kb inversion [36], the 3.3-kb inversion [27] and the D inversion [24] , have at least one of their endpoints located within BZ region. Notably, up to five tRNA genes are concentrated in this small region after the three inversions (Figure 1a). This (...truncated)