Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research

Mueller‐Cajar, Oliver; Whitney, Spencer M.

doi:10.1007/s11120-008-9324-z

Cited by 83 publications

(90 citation statements)

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“…Tradeoffs between acquiring beneficial catalytic changes while maintaining catalytic chemistry and satisfying the many molecular interaction requirements may have limited the capacity of many Rubiscos to evolve improved catalytic prowess (Mueller-Cajar and Whitney, 2008). The survival dependency of photosynthetic organisms on Rubisco functionality, its high expression levels, and its necessity to interact with so many molecular partners (Fig.…”

Section: Is the Evolution Of Rubisco Naturally Constrained?mentioning

confidence: 99%

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

2010

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There is a growing impetus in developing novel strategies to address global concerns regarding food security. As crop productivity gains through traditional breeding begin to lag and arable land becomes scarcer, it seems that we are heading for unsustainable global populations. It has been foreshadowed that global food production will need to rise more than 50% before 2050 to meet the ever-increasing demand. Compounding the problem are the uncertainties of climate change and its impact on agriculture. Strategies to improve crop yield potential have begun to examine aspects of supercharging photosynthesis to drive a new "green revolution." Central to many of these strategies is addressing the limitation of nature's CO 2 -fixing enzyme, Rubisco.The catalytic incorporation of CO 2 into ribulose 1,5-bisphosphate (RuBP) by Rubisco is the first step in the production of carbohydrates by plants, which are used to build biomass and produce energy during growth and development. Despite the pivotal role of Rubisco in linking the inorganic (CO 2 ) and the organic (biomass) phases of the global carbon cycle, it is a slow and confused catalyst, limiting productivity and resource (e.g. water and nutrients) use efficiency in many plants (Long et al., 2006). Understandably, Rubisco has been studied intensively and is a prime target for genetic engineering to improve photosynthetic efficiency (Raines, 2006;Parry et al., 2007). Although the challenge of making a "better Rubisco" has exceeded the grasp and career of many scientists, recent advances indicate that it is not insurmountable. Here, we examine conceptual and technological breakthroughs over the last decade that have identified new and unconventional members of the Rubisco family, revealed molecular aspects of Rubisco biogenesis in plastids and cyanobacteria, advanced our understanding of its catalytic chemistry, and widened our appreciation of the challenges we face to improve Rubisco activity and plant productivity.

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Section: Is the Evolution Of Rubisco Naturally Constrained?mentioning

confidence: 99%

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

2010

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“…Even with considerable variation in amino acid sequence and biological function, key active site residues are conserved across the three clades [113]. This has resulted in a shared activation process and catalytic chemistry that suggests that there are considerable constraints upon modification of enzyme function [114]. One fundamental issue may be that CO 2 directly binds to the RuBP enediol, rather than forming a Michaelis complex with Rubisco, which reduces the capacity for discrimination against O 2 binding [115].…”

Section: Question 5: How Does Evolutionary History Impact and Inform mentioning

confidence: 99%

Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO ₂ ]

Leakey

Lau

2012

Phil. Trans. R. Soc. B

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Variation in atmospheric [CO 2 ] is a prominent feature of the environmental history over which vascular plants have evolved. Periods of falling and low [CO 2 ] in the palaeo-record appear to have created selective pressure for important adaptations in modern plants. Today, rising [CO 2 ] is a key component of anthropogenic global environmental change that will impact plants and the ecosystem goods and services they deliver. Currently, there is limited evidence that natural plant populations have evolved in response to contemporary increases in [CO 2 ] in ways that increase plant productivity or fitness, and no evidence for incidental breeding of crop varieties to achieve greater yield enhancement from rising [CO 2 ]. Evolutionary responses to elevated [CO 2 ] have been studied by applying selection in controlled environments, quantitative genetics and traitbased approaches. Findings to date suggest that adaptive changes in plant traits in response to future [CO 2 ] will not be consistently observed across species or environments and will not be large in magnitude compared with physiological and ecological responses to future [CO 2 ]. This lack of evidence for strong evolutionary effects of elevated [CO 2 ] is surprising, given the large effects of elevated [CO 2 ] on plant phenotypes. New studies under more stressful, complex environmental conditions associated with climate change may revise this view. Efforts are underway to engineer plants to: (i) overcome the limitations to photosynthesis from today's [CO 2 ] and (ii) benefit maximally from future, greater [CO 2 ]. Targets range in scale from manipulating the function of a single enzyme (e.g. Rubisco) to adding metabolic pathways from bacteria as well as engineering the structural and functional components necessary for C 4 photosynthesis into C 3 leaves. Successfully improving plant performance will depend on combining the knowledge of the evolutionary context, cellular basis and physiological integration of plant responses to varying [CO 2 ].

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“…Identifying the natural changes that result in the faster C 4 rubiscos is far from simple, given the complex structure and biogenesis pathway of the hexadecameric rubisco (L 8 S 8 ) in vascular plants, whose assembly requirements cannot be met by conventional bacterial or in vitro expression systems (15). The catalytic core of L 8 S 8 rubisco comprises four 52-kDa large (L)-subunit pairs which are capped by two sets of 15-kDa small (S)-subunit tetramers that provide structural stability and influence catalysis (16,17).…”

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

Whitney

Sharwood

Orr

et al. 2011

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

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135

138

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Improving global yields of important agricultural crops is a complex challenge. Enhancing yield and resource use by engineering improvements to photosynthetic carbon assimilation is one potential solution. During the last 40 million years C 4 photosynthesis has evolved multiple times, enabling plants to evade the catalytic inadequacies of the CO 2 -fixing enzyme, ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco). Compared with their C 3 ancestors, C 4 plants combine a faster rubisco with a biochemical CO 2 -concentrating mechanism, enabling more efficient use of water and nitrogen and enhanced yield. Here we show the versatility of plastome manipulation in tobacco for identifying sequences in C 4 -rubisco that can be transplanted into C 3 -rubisco to improve carboxylation rate (V C ). Using transplastomic tobacco lines expressing native and mutated rubisco large subunits (L-subunits) from Flaveria pringlei (C 3 ), Flaveria floridana (C 3 -C 4 ), and Flaveria bidentis (C 4 ), we reveal that Met-309-Ile substitutions in the L-subunit act as a catalytic switch between C 4 ( 309 Ile; faster V C , lower CO 2 affinity) and C 3 ( 309 Met; slower V C , higher CO 2 affinity) catalysis. Application of this transplastomic system permits further identification of other structural solutions selected by nature that can increase rubisco V C in C 3 crops. Coengineering a catalytically faster C 3 rubisco and a CO 2 -concentrating mechanism within C 3 crop species could enhance their efficiency in resource use and yield.CO 2 assimilation | rbcL mutagenesis | gas exchange | chloroplast transformation T he future uncertainties of global climate change and estimates of unsustainable population growth have increased the urgency of improving crop yields (1). One possible solution is to "supercharge" photosynthesis by improving the C 3 cycle (2, 3). Although a simple idea, this is a complex challenge that involves several possible alternatives. Many of these alternatives focus on enhancing the performance of the CO 2 -fixing enzyme ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (rubisco), which catalyses the first step in the synthesis of carbohydrates. Despite its pivotal role, rubisco is a slow catalyst, completing only one to four carboxylation reactions per catalytic site per second in plants (4, 5). Moreover CO 2 not only is fixed through a complex catalytic process but also must compete with O 2 . The oxygenation of RuBP produces 2-phosphoglycolate, whose recycling by photorespiration requires energy and results in the futile loss of fixed carbon [∼30% of fixed CO 2 in many C 3 plants (6)].To compensate for rubisco's catalytic limitations, plants invest as much as 25% of their leaf nitrogen in rubisco (7). This value is much lower in C 4 plants, where a biochemical CO 2 -concentrating mechanism (CCM) elevates CO 2 around rubisco. This optimized microenvironment allows rubisco to operate close to its maximal activity, reducing O 2 competition. This CCM has enabled C 4 plants to evolve rubiscos with substantially im...

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Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research

Cited by 83 publications

References 84 publications

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO ₂ ]

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

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Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research

Cited by 83 publications

References 84 publications

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO 2 ]

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

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Product

Resources

About

Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO ₂ ]

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