Plant growth responses to elevated atmospheric CO<sub>2</sub>are increased by phosphorus sufficiency but not by arbuscular mycorrhizas

Jakobsen, Iver; Smith, Sally E.; Smith, F. A.; Watts‐Williams, Stephanie J.; Clausen, Signe Sandbech; Grønlund, Mette

doi:10.1093/jxb/erw383

Cited by 44 publications

(34 citation statements)

References 80 publications

(132 reference statements)

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“…() reported that eCO 2 generally had a positive influence on AMF colonization. However, the effects of eCO 2 and P supply on the AMF varies with the host plant type, AMF species and climate factors, as well as soil biology and chemistry (Jakobsen et al ., ). Here, we report that growth under eCO 2 significantly improved AMF development on tomato roots, especially under P starvation conditions (Figs b, S1c).…”

Section: Discussionmentioning

confidence: 97%

A novel CO₂‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

Zhou

Jin

et al. 2019

New Phytologist

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Summary Elevated atmospheric carbon dioxide (eCO2) concentrations promote symbiosis between roots and arbuscular mycorrhizal fungi (AMF), modifying plant nutrient acquisition and cycling of carbon, nitrogen and phosphate. However, the biological mechanisms by which plants transmit aerial eCO2 cues to roots, to alter the symbiotic associations remain unknown. We used a range of interdisciplinary approaches, including gene silencing, grafting, transmission electron microscopy, liquid chromatography tandem mass spectrometry (LC–MS/MS), biochemical methodologies and gene transcript analysis to explore the complexities of environmental signal transmission from the point of perception in the leaves at the apex to the roots. Here we show that eCO2 triggers apoplastic hydrogen peroxide (H2O2)‐dependent auxin production in tomato shoots followed by systemic signaling that results in strigolactone biosynthesis in the roots. This redox‐auxin‐strigolactone systemic signaling cascade facilitates eCO2‐induced AMF symbiosis and phosphate utilization. Our results challenge the current paradigm of eCO2 effects on AMF and provide new insights into potential targets for manipulation of AMF symbiosis for high nutrient utilization under future climate change scenarios.

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Section: Discussionmentioning

confidence: 97%

A novel CO₂‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

Zhou

Jin

et al. 2019

New Phytologist

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“…Indeed, N 2 fixation (Fig. Greater access to C (Tissue et al 1996, Hungate et al 1999Fitter et al 2000, de Graaff et al 2006, Cernusak et al 2011, Jakobsen et al 2016, Terrer et al 2016) and stoichiometric demand for N and P (Barrett et al 1998, Niu et al 2013) likely led to the observed increase in nutrient acquisition strategies under elevated CO 2 . 4), and AM colonization (Fig.…”

Section: Discussionmentioning

confidence: 99%

Nutrient acquisition strategies augment growth in tropical N₂‐fixing trees in nutrient‐poor soil and under elevated CO₂

Nasto

Winter

Turner

et al. 2019

Ecology

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Tropical forests play a dominant role in the global carbon (C) cycle, and models predict increases in tropical net primary productivity (NPP) and C storage in response to rising atmospheric carbon dioxide (CO2) concentrations. The extent to which increasing CO2 will enhance NPP depends in part on the availability of nitrogen (N) and phosphorus (P) to support growth. Some tropical trees can potentially overcome nutrient limitation by acquiring N via symbiotic dinitrogen (N2) fixation, which may provide a benefit in acquiring P via investment in N‐rich phosphatase enzymes or arbuscular mycorrhizal (AM) fungi. We conducted a seedling experiment to investigate the effects of elevated CO2 and soil nutrient availability on the growth of two N2‐fixing and two non‐N2‐fixing tropical tree species. We hypothesized that under elevated CO2 and at low nutrient availability (i.e., low N and P), N2 fixers would have higher growth rates than non‐N2 fixers because N2 fixers have a greater capacity to acquire both N and P. We also hypothesized that differences in growth rates between N2 fixers and non‐N2 fixers would decline as nutrient availability increases because N2 fixers no longer have an advantage in nutrient acquisition. We found that the N2 fixers had higher growth rates than the non‐N2 fixers under elevated CO2 and at low nutrient availability, and that the difference in growth rates between the N2 and non‐N2 fixers declined as nutrient availability increased, irrespective of CO2. Overall, N2 fixation, root phosphatase activity, and AM colonization decreased with increasing nutrient availability, and increased under elevated CO2 at low nutrient availability. Further, AM colonization was positively related to the growth of the non‐N2 fixers, whereas both N2 fixation and root phosphatase activity were positively related to the growth of the N2 fixers. Though our results indicate all four tree species have the capacity to up‐ or down‐regulate nutrient acquisition to meet their stoichiometric demands, the greater capacity for the N2 fixers to acquire both N and P may enable them to overcome nutritional constraints to NPP under elevated CO2, with implications for the response of tropical forests to future environmental change.

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“…The M. truncatula Jemalong A17 ecotype is commonly used as the model for the study of many aspects of the mycorrhizal symbiosis, from whole plant physiology through to questions of fundamental plant biology (Jakobsen et al, ; Javot, Penmetsa, Terzaghi, Cook, & Harrison, ). This ecotype is generally characterized by vigorous colonization by AMF and large positive mycorrhizal growth responses in response to abiotic stresses such as nutrient deficiency/toxicity (Watts‐Williams et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, the variation in the noninoculated plants in the present study was much higher than that found by Sutka et al (), suggesting that M. truncatula has the capacity for a wider range of water transport than A. thaliana . However, M. truncatula can be very responsive in terms of physiology (e.g., growth and nutrient uptake) to AMF inoculation (Jakobsen et al, ; Watts‐Williams, Jakobsen, Cavagnaro, & Grønlund, ) and thus may often associate with AMF in its natural environment; therefore, the lower variation in L o observed in the inoculated plants may be more representative of the “natural” state for M. truncatula , and those noninoculated accessions that have very low L o (Libya and A17) may be particularly affected by the lack of AMF inoculation.…”

Section: Discussionmentioning

confidence: 99%

Variable effects of arbuscular mycorrhizal fungal inoculation on physiological and molecular measures of root and stomatal conductance of diverse Medicago truncatula accessions

Watts‐Williams

Cavagnaro

Tyerman

2018

Plant Cell & Environment

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Association with arbuscular mycorrhizal fungi (AMF) can impact on plant water relations; mycorrhizal plants can exhibit increased stomatal conductance (g ) and root hydraulic conductance (normalized to root dry weight, L ), and altered expression of aquaporins (AQP). Many factors regulate such responses; however, plant intraspecific diversity effects have yet to be explored. Twenty geographically diverse accessions of Medicago truncatula were inoculated with the AMF Funneliformis mosseae or mock-inoculated, and grown under well-watered conditions. Biomass, g , shoot nutrient concentrations and mycorrhizal colonization were measured in all accessions, and L and gene expression in five accessions. The diverse accessions varied in physiology and gene expression; some accessions were also larger or had higher g when colonized by F. mosseae. In the five accessions, L was higher in two accessions when colonized by AMF and also maintained within a much smaller range than the mock-inoculated plants. Expression of MtPIP1 correlated with both g and L , and when plants were more than 3% colonized, mycorrhizal colonization correlated with L . Accession and AMF treatments had profound effects on M. truncatula, including several measures of plant water relations. Correlations between response variables, especially between molecular and physiological variables, across genotypes, highlight the findings of this study.

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Plant growth responses to elevated atmospheric CO₂are increased by phosphorus sufficiency but not by arbuscular mycorrhizas

Abstract: HighlightExperiments combining elevated CO2 (eCO2), mycorrhizas and soil P level revealed that eCO2 increases the P use efficiency in Medicago truncatula and Brachypodium distachyon but not their mycorrhiza-mediated P uptake.

Cited by 44 publications

References 80 publications

A novel CO₂‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

A novel CO₂‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

Nutrient acquisition strategies augment growth in tropical N₂‐fixing trees in nutrient‐poor soil and under elevated CO₂

Variable effects of arbuscular mycorrhizal fungal inoculation on physiological and molecular measures of root and stomatal conductance of diverse Medicago truncatula accessions

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Plant growth responses to elevated atmospheric CO2are increased by phosphorus sufficiency but not by arbuscular mycorrhizas

Abstract: HighlightExperiments combining elevated CO2 (eCO2), mycorrhizas and soil P level revealed that eCO2 increases the P use efficiency in Medicago truncatula and Brachypodium distachyon but not their mycorrhiza-mediated P uptake.

Cited by 44 publications

References 80 publications

A novel CO2‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

A novel CO2‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

Nutrient acquisition strategies augment growth in tropical N2‐fixing trees in nutrient‐poor soil and under elevated CO2

Variable effects of arbuscular mycorrhizal fungal inoculation on physiological and molecular measures of root and stomatal conductance of diverse Medicago truncatula accessions

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Plant growth responses to elevated atmospheric CO₂are increased by phosphorus sufficiency but not by arbuscular mycorrhizas

A novel CO₂‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

A novel CO₂‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

Nutrient acquisition strategies augment growth in tropical N₂‐fixing trees in nutrient‐poor soil and under elevated CO₂