Hybrid Rubisco of tomato large subunits and tobacco small subunits is functional in tobacco plants

Zhang, Xing‐Hai; Webb, James; Huang, Yan; Li, Lin; Risheng, Tang; Liu, Aimin

doi:10.1016/j.plantsci.2010.11.001

Cited by 32 publications

(18 citation statements)

References 58 publications

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“…Previous studies of hybrid Rubiscos comprising plant L-subunits have shown the pervasive role of the L-subunit on shaping catalysis (13,14,28). Here, a modest yet significant reduction in k C cat and improvement in K C was found for the L 8 A S 8 t Rubisco relative to the native Arabidopsis and tobacco enzymes, which have comparable catalytic constants at 25°C (Table S1).…”

Section: Discussionmentioning

confidence: 53%

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone

Whitney

Birch

Kelso

et al. 2015

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

108

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Enabling improvements to crop yield and resource use by enhancing the catalysis of the photosynthetic CO 2 -fixing enzyme Rubisco has been a longstanding challenge. Efforts toward realization of this goal have been greatly assisted by advances in understanding the complexities of Rubisco's biogenesis in plastids and the development of tailored chloroplast transformation tools. Here we generate transplastomic tobacco genotypes expressing Arabidopsis Rubisco large subunits (AtL), both on their own (producing tob AtL plants) and with a cognate Rubisco accumulation factor 1 (AtRAF1) chaperone (producing tob plants) that has undergone parallel functional coevolution with AtL. We show AtRAF1 assembles as a dimer and is produced in tob and Arabidopsis leaves at 10-15 nmol AtRAF1 monomers per square meter. Consistent with a postchaperonin large (L)-subunit assembly role, the AtRAF1 facilitated two to threefold improvements in the amount and biogenesis rate of hybrid L 8 A S 8 t Rubisco [comprising AtL and tobacco small (S) subunits] in tob AtL-R1 leaves compared with tob AtL , despite >threefold lower steady-state Rubisco mRNA levels in tob . Accompanying twofold increases in photosynthetic CO 2 -assimilation rate and plant growth were measured for tob lines. These findings highlight the importance of ancillary protein complementarity during Rubisco biogenesis in plastids, the possible constraints this has imposed on Rubisco adaptive evolution, and the likely need for such interaction specificity to be considered when optimizing recombinant Rubisco bioengineering in plants.T he increasing global demands for food supply, bioenergy production, and CO 2 -sequestration have placed a high need on improving agriculture yields and resource use (1, 2). It is now widely recognized that yield increases are possible by enhancing the light harvesting and CO 2 -fixation processes of photosynthesis (3-5). A major target for improvement is the enzyme Rubisco [ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase] whose deficiencies in CO 2 -fixing speed and efficiency pose a key limitation to photosynthetic CO 2 capture (6, 7). In plants, the complex, multistep catalytic mechanism of Rubisco to bind its 5-carbon substrate RuBP, orient its C-2 for carboxylation, and then process the 6-carbon product into two 3-phosphoglycerate (3PGA) products, limits its throughput to one to four catalytic cycles per second (8). The mechanism also makes Rubisco prone to competitive inhibition by O 2 that produces only one 3PGA and 2-phosphoglycolate (2PG). Metabolic recycling of 2PG by photorespiration requires energy and results in most plants losing 30% of their fixed CO 2 (5). To compensate for these catalytic limitations, plants like rice and wheat invest up to 50% of the leaf protein into Rubisco, which accounts for ∼25% of their leaf nitrogen (9).Natural diversity in Rubisco catalysis demonstrates that plant Rubisco is not the pinnacle of evolution (6, 7). Better-performing versions in some red algae have the potential to raise the yield of ...

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Section: Discussionmentioning

confidence: 53%

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone

Whitney

Birch

Kelso

et al. 2015

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

108

View full text Add to dashboard Cite

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“…Experimentally testing these predictions, identifying other catalytically determinant L-subunit residues, and exploring which particular rubiscos are affected by these changes have been hampered by the preferential location of rbcL in the plastome (27) and the small range of species whose plastomes can be transformed stably (28). However, as shown in this and previous studies (24,29,30), these experimental limitations may be circumvented by expressing hybrid rubiscos in tobacco plastids. The generality of this system for examining sequence-performance relationships within otherwise inaccessible, catalytically diverse foreign L-subunits remains to be explored fully.…”

Section: Discussionmentioning

confidence: 95%

“…The apparent catalytic neutrality of the tobacco S-subunit when assembled with heterologous L-subunits (Fig. 3) (24,29,30) contrasts with the recent success in shaping rice rubisco toward C 4 -like catalysis using heterologous S-subunits from C 4 sorghum (16). Similarly, structural changes to the S-subunit have improved Chlamydomonas rubisco catalysis (17).…”

Section: Discussionmentioning

confidence: 97%

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.

132

135

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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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“…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). In some cases, the plants were able to grow also autotrophically under normal (Zhang et al 2011) or special atmospheric conditions (elevated CO 2 content) (e.g., Kanevski et al 1999;Alonso et al 2009;Sharwood et al 2008;reviewed in Hanson et al 2013).…”

Section: Attempts To Influence Crop Productivitymentioning

confidence: 99%

“…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). In some cases, the plants were able to grow also autotrophically under normal (Zhang et al 2011) or special atmospheric conditions (elevated CO 2 content) (e.g., Kanevski et al 1999;Alonso et al 2009;Sharwood et al 2008;reviewed in Hanson et al 2013). The low mRNA level, translation, and/or macrodomain assembly of the foreign rbcL gene is probably the reason of the observed decreased functionality in the transplastomic plants .…”

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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Hybrid Rubisco of tomato large subunits and tobacco small subunits is functional in tobacco plants

Cited by 32 publications

References 58 publications

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone

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

Transplastomic plants for innovations in agriculture. A review

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Hybrid Rubisco of tomato large subunits and tobacco small subunits is functional in tobacco plants

Cited by 32 publications

References 58 publications

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone

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

Transplastomic plants for innovations in agriculture. A review

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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