Adaptive evolution of rbcL in Conocephalum (Hepaticae, bryophytes)

Miwa, Hidetsugu; Odrzykoski, Ireneusz J.; Matsui, Atsushi; Hasegawa, Masami; Akiyama, Hiroyuki; Jia, Yu; Сабиров, Р Н; Takahashi, Hideki; Boufford, David E.; Murakami, Noriaki

doi:10.1016/j.gene.2008.11.020

Cited by 29 publications

(14 citation statements)

References 30 publications

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“…The initial molecular-phylogenetic analysis of rbcL showed that positive selection is widespread among all main lineages of land plants, but is restricted to a relatively small number of Rubisco amino acid residues within functionally important sites [6]. Following studies showed that rbcL is under positive selection in particular taxonomic groups [26], [27], [51], [52], [53], [54], [55], [56]. Coevolution of residues is common in Rubisco of land plants as well as positive selection and there is an overlap between coevolving and positively selected residues [57].…”

Section: Discussionmentioning

confidence: 99%

Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

2012

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BackgroundRubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) catalyses the key reaction in the photosynthetic assimilation of CO2. In C4 plants CO2 is supplied to Rubisco by an auxiliary CO2-concentrating pathway that helps to maximize the carboxylase activity of the enzyme while suppressing its oxygenase activity. As a consequence, C4 Rubisco exhibits a higher maximum velocity but lower substrate specificity compared with the C3 enzyme. Specific amino-acids in Rubisco are associated with C4 photosynthesis in monocots, but it is not known whether selection has acted on Rubisco in a similar way in eudicots.Methodology/Principal FindingsWe investigated Rubisco evolution in Amaranthaceae sensu lato (including Chenopodiaceae), the third-largest family of C4 plants, using phylogeny-based maximum likelihood and Bayesian methods to detect Darwinian selection on the chloroplast rbcL gene in a sample of 179 species. Two Rubisco residues, 281 and 309, were found to be under positive selection in C4 Amaranthaceae with multiple parallel replacements of alanine by serine at position 281 and methionine by isoleucine at position 309. Remarkably, both amino-acids have been detected in other C4 plant groups, such as C4 monocots, illustrating a striking parallelism in molecular evolution.Conclusions/SignificanceOur findings illustrate how simple genetic changes can contribute to the evolution of photosynthesis and strengthen the hypothesis that parallel amino-acid replacements are associated with adaptive changes in Rubisco.

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Section: Discussionmentioning

confidence: 99%

Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

2012

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“…situations where morphology-based taxonomy is challenging, or has not been done thoroughly). One plant group in which DNA barcoding approaches are providing useful insights into cryptic species diversity is bryophytes ([84], [85] Hollingsworth et al unpublished). Bryophyte species in general lack many of the ‘problem’ features outlined in Table 2.…”

Section: Applications Of Dna Barcoding In Plantsmentioning

confidence: 99%

Choosing and Using a Plant DNA Barcode

2011

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The main aim of DNA barcoding is to establish a shared community resource of DNA sequences that can be used for organismal identification and taxonomic clarification. This approach was successfully pioneered in animals using a portion of the cytochrome oxidase 1 (CO1) mitochondrial gene. In plants, establishing a standardized DNA barcoding system has been more challenging. In this paper, we review the process of selecting and refining a plant barcode; evaluate the factors which influence the discriminatory power of the approach; describe some early applications of plant barcoding and summarise major emerging projects; and outline tool development that will be necessary for plant DNA barcoding to advance.

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“…at the genus level) [89] . On the other respect, the molecular adaptation in rbcL gene per se also has impact on the inferring of the phylogenetic trees [17] . The above two factors may be the explanation for the disagreement between the inferred tree topology and the taxonomic classification .…”

Section: Reviewers' Commentsmentioning

confidence: 99%

“…Significant positive selection events have been also identified in the RbcL subunit of most land plant lineages by using simulation approaches [15]. In particular, the adaptive evolution of rbcL genes has been found in the aquatic plant Potamogeton [16] and the F-type lineage of Conocephalum [17]. These findings make it plausible to hypothesize that RbcL subunit may have undergone "continual fine-tuning" in green plants to adapt to CO 2 concentration changes across geological epochs [18].…”

Section: Introductionmentioning

confidence: 99%

Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns

et al. 2011

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BackgroundThe chloroplast-localized ribulose-1, 5-biphosphate carboxylase/oxygenase (Rubisco), the primary enzyme responsible for autotrophy, is instrumental in the continual adaptation of plants to variations in the concentrations of CO2. The large subunit (LSU) of Rubisco is encoded by the chloroplast rbcL gene. Although adaptive processes have been previously identified at this gene, characterizing the relationships between the mutational dynamics at the protein level may yield clues on the biological meaning of such adaptive processes. The role of such coevolutionary dynamics in the continual fine-tuning of RbcL remains obscure.ResultsWe used the timescale and phylogenetic analyses to investigate and search for processes of adaptive evolution in rbcL gene in three gymnosperm families, namely Podocarpaceae, Taxaceae and Cephalotaxaceae. To understand the relationships between regions identified as having evolved under adaptive evolution, we performed coevolutionary analyses using the software CAPS. Importantly, adaptive processes were identified at amino acid sites located on the contact regions among the Rubisco subunits and on the interface between Rubisco and its activase. Adaptive amino acid replacements at these regions may have optimized the holoenzyme activity. This hypothesis was pinpointed by evidence originated from our analysis of coevolution that supported the correlated evolution between Rubisco and its activase. Interestingly, the correlated adaptive processes between both these proteins have paralleled the geological variation history of the concentration of atmospheric CO2.ConclusionsThe gene rbcL has experienced bursts of adaptations in response to the changing concentration of CO2 in the atmosphere. These adaptations have emerged as a result of a continuous dynamic of mutations, many of which may have involved innovation of functional Rubisco features. Analysis of the protein structure and the functional implications of such mutations put forward the conclusion that this evolutionary scenario has been possible through a complex interplay between adaptive mutations, often structurally destabilizing, and compensatory mutations. Our results unearth patterns of evolution that have likely optimized the Rubisco activity and uncover mutational dynamics useful in the molecular engineering of enzymatic activities.ReviewersThis article was reviewed by Prof. Christian Blouin (nominated by Dr W Ford Doolittle), Dr Endre Barta (nominated by Dr Sandor Pongor), and Dr Nicolas Galtier.

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Adaptive evolution of rbcL in Conocephalum (Hepaticae, bryophytes)

Cited by 29 publications

References 30 publications

Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

Choosing and Using a Plant DNA Barcode

Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns

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