Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection

Souza, Amanda P. De; Burgess, Steven J.; Doran, Lynn; Hansen, Jeffrey; Manukyan, Lusya; Maryn, Nina; Gotarkar, Dhananjay; Leonelli, Lauriebeth; Niyogi, Krishna; Long, Stephen P.

doi:10.1126/science.adc9831

Cited by 203 publications

(154 citation statements)

References 45 publications

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“…Therefore, the finding of faster recovery of ΦPSII conveyed by the Bur-0 plasmotype to be associated with faster relaxation of ΦNPQ implies there is not merely a difference in activation of NPQ but also in actual dissipation. Hence the variation causal to the faster recovery of ΦPSII is promising for potential photosynthetic improvements, as has been experimentally shown (Kromdijk et al, 2016;De Souza et al, 2022).…”

Section: Discussionmentioning

confidence: 87%

The NDH complex reveals a trade-off that constrains maximising photosynthesis inArabidopsis thaliana

Theeuwen

Lawson

Tijink

et al. 2022

Preprint

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The Green Revolution has resulted in major improvements in crop productivity, but left photosynthesis largely unimproved. Despite ample variation of photosynthetic performance in crops and their wild relatives, the photosynthetic capacity of elite breeding lines remains well below its theoretical maximum. As yield is often the primary selective trait, current plant breeding approaches result in photosynthetic trade-offs that prevent positive selection for photosynthetic performance itself. Currently, genetic variation for photosynthetic performance is seldomly validated at the genetic level, and as a result these photosynthetic trade-offs remain poorly understood. Here we reveal the physiological nature of a photosynthetic trade-off caused by the NAD(P)H dehydrogenase (NDH) complex. The use of an Arabidopsis thaliana cybrid panel revealed how a natural allele of the chloroplastic gene NAD(P)H-QUINONE OXIDOREDUCTASE SUBUNIT 6 - a subunit of the NDH complex - results in a faster recovery of photosystem II efficiency after a transition from high to low irradiances. This improvement is due to a reduction in NDH activity. Under low-light conditions this reduction in NDH activity has a neutral effect on biomass, while under highly fluctuating light conditions, including high irradiances, more NDH activity is favoured. This shows that while allelic variation in one gene can have beneficial effects on one aspect of photosynthesis, it can, depending on environmental conditions, have negative effects on other aspects of photosynthesis. As environmental conditions are hardly ever stable in agricultural systems, understanding photosynthetic trade-offs allows us to explore shifting photosynthetic performance closer to the theoretical maximum.

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Section: Discussionmentioning

confidence: 87%

The NDH complex reveals a trade-off that constrains maximising photosynthesis inArabidopsis thaliana

Theeuwen

Lawson

Tijink

et al. 2022

Preprint

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“…Chen et al (2019) introduced exogenous glycolate catabolic pathway into cucumber and obtained transgenic plants that can exhibit high photosynthetic efficiency under low-CO 2 environment. De Souza et al (2022) overexpressed VPZ gene in soybean, which effectively improved the efficiency of photosynthesis. Specifically, it resulted in a 33% increase in soybean yield (De Souza et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…De Souza et al (2022) overexpressed VPZ gene in soybean, which effectively improved the efficiency of photosynthesis. Specifically, it resulted in a 33% increase in soybean yield (De Souza et al, 2022). However, with overexpression of SBP or FBA in plants, the improvements in photosynthesis and biomass yield occurred only under elevated CO 2 conditions (Rosenthal et al, 2011;Uematsu et al, 2012), such improvements are significant in greenhouse environments in winter (Rosenthal et al, 2011), the authors of these studies attribute the results to the shorter day length and the lower light level.…”

Section: Discussionmentioning

confidence: 99%

Multigene manipulation of photosynthetic carbon metabolism enhances the photosynthetic capacity and biomass yield of cucumber under low-CO2 environment

Chen

Wang²,

Feng³

et al. 2022

Front. Plant Sci.

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Solar greenhouses are important in the vegetable production and widely used for the counter-season production in the world. However, the CO2 consumed by crops for photosynthesis after sunrise is not supplemented and becomes chronically deficient due to the airtight structure of solar greenhouses. Vegetable crops cannot effectively utilize light resources under low-CO2 environment, and this incapability results in reduced photosynthetic efficiency and crop yield. We used cucumber as a model plant and generated several sets of transgenic cucumber plants overexpressing individual genes, including β-carbonic anhydrase 1 (CsβCA1), β-carbonic anhydrase 4 (CsβCA4), and sedoheptulose-1,7-bisphosphatase (CsSBP); fructose-1,6-bisphosphate aldolase (CsFBA), and CsβCA1 co-expressing plants; CsβCA4, CsSBP, and CsFBA co-expressing plants (14SF). The results showed that the overexpression of CsβCA1, CsβCA4, and 14SF exhibited higher photosynthetic and biomass yield in transgenic cucumber plants under low-CO2 environment. Further enhancements in photosynthesis and biomass yield were observed in 14SF transgenic plants under low-CO2 environment. The net photosynthesis biomass yield and photosynthetic rate increased by 49% and 79% compared with those of the WT. However, the transgenic cucumbers of overexpressing CsFBA and CsSBP showed insignificant differences in photosynthesis and biomass yield compared with the WT under low-CO2.environment. Photosynthesis, fluorescence parameters, and enzymatic measurements indicated that CsβCA1, CsβCA4, CsSBP, and CsFBA had cumulative effects in photosynthetic carbon assimilation under low-CO2 environment. Co-expression of this four genes (CsβCA1, CsβCA4, CsSBP, and CsFBA) can increase the carboxylation activity of RuBisCO and promote the regeneration of RuBP. As a result, the 14SF transgenic plants showed a higher net photosynthetic rate and biomass yield even under low-CO2environment.These findings demonstrate the possibility of cultivating crops with high photosynthetic efficiency by manipulating genes involved in the photosynthetic carbon assimilation metabolic pathway.

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“…The energy losses due to photosynthesis regulatory mechanisms can be particularly impactful in the case of light fluctuations, when NPQ and the xanthophyll cycle are activated during light peaks and remain active when the illumination decreases. In plants it has been shown that accelerating the kinetics of the xanthophyll cycle can lead to a remarkable increase in photosynthetic productivity in the field (14,15). Unicellular algae, like all other photosynthetic organisms, are exposed to light fluctuations in nature and have multiple mechanisms to modulate their photosynthetic efficiency, including NPQ and the xanthophyll cycle (16,17).…”

Section: Introductionmentioning

confidence: 99%

Modulation of xanthophyll cycle impacts biomass productivity in the marine microalgaNannochloropsis

Perin

Bellan

Lyska

et al. 2022

Preprint

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Life on earth depends on photosynthetic primary producers that exploit sunlight to fix CO2 into biomass. Approximately half of global primary production is associated with microalgae living in aquatic environments. Microalgae also represent a promising source of biomass to complement crop cultivation, and they could contribute to the development of a more sustainable bioeconomy. Photosynthetic organisms evolved multiple mechanisms involved in the regulation of photosynthesis to respond to highly variable environmental conditions. While essential to avoid photodamage, regulation of photosynthesis results in dissipation of absorbed light energy, generating a complex trade-off between protection from stress and light-use efficiency. This work investigates the impact of the xanthophyll cycle, the light-induced reversible conversion of violaxanthin into zeaxanthin, on the protection from excess light and on biomass productivity in the marine microalgae of the genus Nannochloropsis. Zeaxanthin is shown to have an essential role in protection from excess light, contributing to the induction of Non-Photochemical Quenching and scavenging of reactive oxygen species. On the other hand, the overexpression of Zeaxanthin Epoxidase, enables a faster re-conversion of zeaxanthin to violaxanthin that is shown to be advantageous for biomass productivity in dense cultures in photobioreactors. These results demonstrate that zeaxanthin accumulation is critical to respond to strong illumination, but it may lead to unnecessary energy losses in light-limiting conditions, and accelerating its re-conversion to violaxanthin provides an advantage for biomass productivity in microalgae.

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Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection

Cited by 203 publications

References 45 publications

The NDH complex reveals a trade-off that constrains maximising photosynthesis inArabidopsis thaliana

The NDH complex reveals a trade-off that constrains maximising photosynthesis inArabidopsis thaliana

Multigene manipulation of photosynthetic carbon metabolism enhances the photosynthetic capacity and biomass yield of cucumber under low-CO2 environment

Modulation of xanthophyll cycle impacts biomass productivity in the marine microalgaNannochloropsis

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