Isoleucine 309 acts as a C
            <sub>4</sub>
            catalytic switch that increases ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in
            <i>Flaveria</i>

Whitney, Spencer M.; Sharwood, Robert E.; Orr, Douglas J.; White, Sarah; Alonso, Hernán; Galmés, Jeroni

doi:10.1073/pnas.1109503108

Cited by 132 publications

(138 citation statements)

References 36 publications

(70 reference statements)

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“…Those mutations near the dimer or N-and C-terminal domain interfaces within each large subunit likely affect the substantial relative movements of the domains on substrate binding. Although one of these residue changes (M309I) has previously been shown to switch the enzyme to C 4 -like properties in plants (21), it is clear that this change is not essential, and there are other mutational routes to equivalent functional changes. Negative cooperativity has been reported for the binding of the transition-state analog 2-carboxyarabinitol bisphosphate to the active site of the C 3 RubisCO from spinach (33).…”

Section: Discussionmentioning

confidence: 99%

“…Another frequently positively selected mutation, M309I, also identified in some previous phylogenetic studies (20,24), lies at the interface of the two C-terminal domains within a dimer and also close to the junction between N-and C-terminal domains within each subunit. This mutation has been demonstrated to act as a catalytic switch between C 3 -like and C 4 -like properties (i.e., decreasing specificity for CO 2 over O 2 and increasing the turnover) in Flaveria species and in chimeric enzymes consisting of large subunits from Flaveria and tobacco small subunits (21). However, isoleucine is present in only half of all of the C 4 forms.…”

Section: Analysis Of Mutations Occurring During Evolution and Their Ementioning

confidence: 99%

“…Experimental studies of RubisCOs from very closely related C 3 and C 4 species within the Flaveria, Atriplex, and Neurachne genera showed that very few changes may be necessary to modify enzymatic properties in response to the modification of the metabolic context (19,20). Indeed, in the Flaveria context, a single mutation (M309I) has been identified as key in modifying specificity and increasing turnover (21); it remains unclear as to how this observation applies to a wider range of plants and what the contributions are of other observed mutations to adaptation. Comparative sequence analysis of a broader range of plant species does suggest that, in general, adaptation of RubisCO to C 4 metabolism involves a larger number of amino acid changes found to be under positive selection (19,20).…”

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confidence: 99%

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Stability-activity tradeoffs constrain the adaptive evolution of RubisCO

Studer

Christin

Williams

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

142

137

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A well-known case of evolutionary adaptation is that of ribulose-1,5-bisphosphate carboxylase (RubisCO), the enzyme responsible for fixation of CO 2 during photosynthesis. Although the majority of plants use the ancestral C 3 photosynthetic pathway, many flowering plants have evolved a derived pathway named C 4 photosynthesis. The latter concentrates CO 2 , and C 4 RubisCOs consequently have lower specificity for, and faster turnover of, CO 2 . The C 4 forms result from convergent evolution in multiple clades, with substitutions at a small number of sites under positive selection. To understand the physical constraints on these evolutionary changes, we reconstructed in silico ancestral sequences and 3D structures of RubisCO from a large group of related C 3 and C 4 species. We were able to precisely track their past evolutionary trajectories, identify mutations on each branch of the phylogeny, and evaluate their stability effect. We show that RubisCO evolution has been constrained by stability-activity tradeoffs similar in character to those previously identified in laboratory-based experiments. The C 4 properties require a subset of several ancestral destabilizing mutations, which from their location in the structure are inferred to mainly be involved in enhancing conformational flexibility of the open-closed transition in the catalytic cycle. These mutations are near, but not in, the active site or at intersubunit interfaces. The C 3 to C 4 transition is preceded by a sustained period in which stability of the enzyme is increased, creating the capacity to accept the functionally necessary destabilizing mutations, and is immediately followed by compensatory mutations that restore global stability.T he adaptive diversification of organisms often requires the evolution of novel enzymatic properties. The evolutionary shift from one enzymatic function to another involves crossing an energetic barrier in a fitness landscape (1). The number of mutations that confer advantageous function during such a shift is consequently limited. Some residues are critical for maintaining the stability of the protein fold, others are important for the catalytic activity itself. Due to the multiple roles of amino acids in proteins, the adaptation of one physical parameter of an enzyme is likely to affect other properties (2). As proteins usually form thermodynamically stable structures, their evolutionary trajectories are constrained to a narrow range of stability (3). Stability and activity are likely to be negatively correlated. Most possible amino acid changes in native proteins are destabilizing and, consequently, mutations that lead to a more favorable enzyme activity are likely to decrease the stability of the protein (2, 4). Compensatory mutations are then needed to restore global stability. These processes are referred to as stability-activity tradeoffs (5-7). Furthermore, proteins with higher stability confer greater evolvability, because there is more scope to accept destabilizing yet functionally beneficial changes (8). Wh...

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Section: Discussionmentioning

confidence: 99%

Section: Analysis Of Mutations Occurring During Evolution and Their Ementioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Stability-activity tradeoffs constrain the adaptive evolution of RubisCO

Studer

Christin

Williams

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

142

137

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“…In other studies, the introduction of large subunit transgenes into the plastome was used to trigger changes between C 3 and C 4 photosynthesis offering great promise in improving crop productivity under changing environmental conditions (Whitney et al 2011b;Galmés et al 2013). Similarly, screening the RuBisCO specificity of several species to find the most efficient enzyme (under given environmental conditions) and transferring it into important crops may lead to an improved net photosynthetic rate by as much as 29 %, at least on the basis of some prediction models and considering unaltered carboxylation rate (Raines 2006).…”

Section: Attempts To Influence Crop Productivitymentioning

confidence: 99%

“…However, the attempts to replace the plastidlocated tobacco RuBisCO large subunit with the same gene from cyanobacteria (Synechococcus- Kanevski et al 1999), proteobacteria (Rhodospirillum rubrum- Andrews 2001b, 2003), archaebacteria (Methanococcoides burtonii- Alonso et al 2009), non-green algae (the rhodophyte Galdieria sulphuraria and the diatom Phaeodactylum tricornutum- Whitney et al 2001), sunflower (Kanevski et al 1999), tomato (Zhang et al 2011), and Flaveria (Whitney et al 2011b;Galmés et al 2013) resulted in general in non-autotrophic transformants. These produced either no RuBisCO, like in case of the Synechococcus gene (Kanevski et al 1999), or had no properly folded proteins with no assembly of the RuBisCO subunits as a result (Whitney et al 2001) or assembled into hybrid RuBisCO hexadecamers which were, however, usually less functional than the enzyme of the non-transformed plants (Kanevski et al 1999;Alonso et al 2009;Zhang et al 2011).…”

Section: Attempts To Influence Crop Productivitymentioning

confidence: 99%

Transplastomic plants for innovations in agriculture. A review

Wani

Sah

Sági

et al. 2015

Agron. Sustain. Dev.

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Food production has to be significantly increased in order to feed the fast growing global population estimated to be 9.1 billion by 2050. The Green Revolution and the development of advanced plant breeding tools have led to a significant increase in agricultural production since the 1960s. However, hundreds of millions of humans are still undernourished, while the area of total arable land is close to its maximum utilization and may even decrease due to climate change, urbanization, and pollution. All these issues necessitate a second Green Revolution, in which biotechnological engineering of economically and nutritionally important traits should be critically and carefully considered. Since the early 1990s, possible applications of plastid transformation in higher plants have been constantly developed. These represent viable alternatives to existing nuclear transgenic technologies, especially due to the better transgene containment of transplastomic plants. Here, we present an overview of plastid engineering techniques and their applications to improve crop quality and productivity under adverse growth conditions. These applications include (1) transplastomic plants producing insecticidal, antibacterial, and antifungal compounds. These plants are therefore resistant to pests and require less pesticides. (2) Transplastomic plants resistant to cold, drought, salt, chemical, and oxidative stress. Some pollution tolerant plants could even be used for phytoremediation. (3) Transplastomic plants having higher productivity as a result of improved photosynthesis. (4) Transplastomic plants with enhanced mineral, micronutrient, and macronutrient contents. We also evaluate field trials, biosafety issues, and public concerns on transplastomic plants. Nevertheless, the transplastomic technology is still unavailable for most staple crops, including cereals. Transplastomic plants have not been commercialized so far, but if this crop limitation were overcome, they could contribute to sustainable development in agriculture.

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