Copper deficiency alters shoot architecture and reduces fertility of both gynoecium and androecium in <i>Arabidopsis thaliana</i>

Ishka, Maryam Rahmati; Vatamaniuk, Olena K.

doi:10.1002/pld3.288

Cited by 26 publications

(21 citation statements)

References 101 publications

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“…A previous study showed that perturbation of sphingolipid biosynthesis in the roots influences the leaf ionome (Chao et al, 2011), and thus, sphingolipids may play consequential roles in both Cu-deficiency and heat stress. Some lignans were also found to be downregulated in Cu-deficient and heat treated plants in both leaves and roots, consistent with previous observations of lignin biosynthesis affected under copper deficiency (Schulten and Krämer, 2018; Rahmati Ishka and Vatamaniuk, 2020).…”

Section: Resultssupporting

confidence: 91%

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Characterization and visualization of global metabolomic responses ofBrachypodium distachyonto environmental changes

Mahood

Bennett

Komatsu

et al. 2022

Preprint

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Plant responses to environmental change are mediated via changes in cellular metabolomes. However, <5% of signals obtained from tandem liquid chromatography mass spectrometry (LC-MS/MS) can be identified, limiting our understanding of how different metabolite classes change under biotic/abiotic stress. To address this challenge, we performed untargeted LC-MS/MS of leaves, roots and other organs of Brachypodium distachyon, a model Poaceae species, under 17 different organ-condition combinations, including copper deficiency, heat stress, low phosphate and arbuscular mycorrhizal symbiosis (AMS). We used a combination of information theory-based metrics and machine learning-based identification of metabolite structural classes to assess metabolomic changes. Both leaf and root metabolomes were significantly affected by the growth medium. Leaf metabolomes were more diverse than root metabolomes, but the latter were more specialized and more responsive to environmental change. We also found that one week of copper deficiency shielded the root metabolome, but not the leaf metabolome, from perturbation due to heat stress. Using a recently published deep learning based method for metabolite class predictions, we analyzed the responsiveness of each metabolite class to environmental change, which revealed significant perturbations of various lipid classes and phenylpropanoids such as cinnamic acids and flavonoids. Co-accumulation analysis further identified condition-specific metabolic biomarkers. Finally, to make these results publicly accessible, we developed a novel visualization platform on the Bioanalytical Resource website, where significantly perturbed metabolic classes can be readily visualized. Overall, our study illustrates how emerging chemoinformatic methods can be applied to reveal novel insights into the dynamic plant metabolome and plant stress adaptation.

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Section: Resultssupporting

confidence: 91%

“…All samples were stored at −80 °C until further processing. We verified that the Cu-deficiency and AMS conditions worked as expected using RT-PCR of previously known condition-specific genes (Rahmati Ishka and Vatamaniuk, 2020) (Supplementary Methods) .…”

Section: Methodssupporting

confidence: 64%

Characterization and visualization of global metabolomic responses ofBrachypodium distachyonto environmental changes

Mahood

Bennett

Komatsu

et al. 2022

Preprint

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“…Moreover, various abiotic stresses, such as heat stress, phosphate starvation, salt stress and drought, lead to increased miR156 levels (Hsieh et al, 2009;Cui et al, 2014;Stief et al, 2014). Elevated Cu levels in aerial tissues compared to rosette leaves in the wild type indicated that Cu allocation to the inflorescence is prioritized, in agreement with the previously established role of Cu in plant fertility, for example in the Cu-binding protein plantacyanin involved in pollen tube guidance (Kim et al, 2003;Dong et al, 2005;Yan et al, 2017;Rahmati Ishka and Vatamaniuk, 2020). This prioritization was to a large extent dependent on SPL7 (Figure 5B).…”

Section: Spl7 and Cu Deficiency In Plant Developmentsupporting

confidence: 67%

Energy status-promoted growth and development of Arabidopsis require copper deficiency response transcriptional regulator SPL7

Schulten

Pietzenuk

Quintana

et al. 2021

Preprint

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Copper (Cu) is a cofactor of around 300 Arabidopsis proteins including photosynthetic and mitochondrial electron transfer chain enzymes critical for ATP production and carbon fixation. Plant acclimation to Cu deficiency requires the transcription factor SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE7 (SPL7). We report that in the wild type and in the spl7-1 mutant, respiratory electron flux via Cu-dependent cytochrome c oxidase remained unaffected under both normal and low-Cu cultivation conditions. Contrary to the wild type, supplementing Cu-deficient media with exogenous sugar failed to stimulate growth of spl7-1. The spl7-1 mutant accumulated carbohydrates including the signaling sugar trehalose 6-phosphate, as well as ATP and NADH, also under normal Cu supply and without sugar supplementation. Late flowering of spl7 1 was in agreement with its attenuated sugar responsiveness. Functional TOR and SnRK1 kinase signaling in spl7-1 suggested against fundamental defects in these energy-signaling hubs. Sequencing of chromatin immunoprecipitates combined with transcriptomics identified direct targets of SPL7-mediated positive regulation, including FE SUPEROXIDE DISMUTASE1 (FSD1), COPPER-DEFICIENCY-INDUCED TRANSCRIPTION FACTOR1 (CITF1) and uncharacterized bHLH23 (CITF2), as well as an enriched upstream GTACTRC motif. In summary, transducing energy availability into growth and reproductive development requires the function of SPL7. Our results could help to increase crop yields, especially on Cu-deficient soils.

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“…In contrast to wild type, no fruit were produced by spl7 plants in 0.5 µM CuSO 4 , indicating that minimal Cu supplementation is required to restore spl7 fertility ( Fig. 2 C ) ( 32 , 33 ). The concentration of Cu in both wild-type and spl7 fruit increased in response to the concentration of Cu supplied to the roots, over a range of 0.5 to 5 µM CuSO 4 ( Fig.…”

Section: Resultsmentioning

confidence: 96%

Explosive seed dispersal depends on SPL7 to ensure sufficient copper for localized lignin deposition via laccases

Pérez-Antón

Schneider

Kroll

et al. 2022

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

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Significance The sudden explosion of seed pods in popping cress ( Cardamine hirsuta ) takes less than 3 ms to accelerate seeds away from the plant. This explosive mechanism relies on polar deposition of the cell-wall polymer lignin. To investigate the genetic basis for polar lignin deposition, we conducted a mutant screen and identified SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE 7 (SPL7)—a transcriptional regulator of copper homeostasis. We discovered three multicopper laccases, LAC4, 11, and 17, that precisely colocalize with, and are required for, the polar deposition of lignin in explosive seed pods. Activity of these three laccases depends on SPL7 to acclimate to copper deficiency. Our findings demonstrate how mineral nutrition is integrated with polar lignin deposition to facilitate dispersal.

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Copper deficiency alters shoot architecture and reduces fertility of both gynoecium and androecium in Arabidopsis thaliana

Abstract: It has been known for decades that the deficiency in the micronutrient copper in alkaline soils compromises plant fertility with the most negative impact on wheat grain production (Broadley et al., 2012;

Cited by 26 publications

References 101 publications

Characterization and visualization of global metabolomic responses ofBrachypodium distachyonto environmental changes

Characterization and visualization of global metabolomic responses ofBrachypodium distachyonto environmental changes

Energy status-promoted growth and development of Arabidopsis require copper deficiency response transcriptional regulator SPL7

Explosive seed dispersal depends on SPL7 to ensure sufficient copper for localized lignin deposition via laccases

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