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Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling.

ABSTRACT: Iron deficiency hampers photosynthesis and is associated with chlorosis. We recently showed that iron deficiency-induced chlorosis depends on phosphorus availability. How plants integrate these cues to control chlorophyll accumulation is unknown. Here, we show that iron limitation downregulates photosynthesis genes in a phosphorus-dependent manner. Using transcriptomics and genome-wide association analysis, we identify two genes, PHT4;4 encoding a chloroplastic ascorbate transporter and bZIP58, encoding a nuclear transcription factor, which prevent the downregulation of photosynthesis genes leading to the stay-green phenotype under iron-phosphorus deficiency. Joint limitation of these nutrients induces ascorbate accumulation by activating expression of an ascorbate biosynthesis gene, VTC4, which requires bZIP58. Furthermore, we demonstrate that chloroplastic ascorbate transport prevents the downregulation of photosynthesis genes under iron-phosphorus combined deficiency through modulation of ROS homeostasis. Our study uncovers a ROS-mediated chloroplastic retrograde signaling pathway to adapt photosynthesis to nutrient availability.

SUBMITTER: Nam HI

PROVIDER: S-EPMC8664907 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling.

Nam Hye-In HI Shahzad Zaigham Z Dorone Yanniv Y Clowez Sophie S Zhao Kangmei K Bouain Nadia N Lay-Pruitt Katerina S KS Cho Huikyong H Rhee Seung Y SY Rouached Hatem H

Nature communications 20211210 1

Iron deficiency hampers photosynthesis and is associated with chlorosis. We recently showed that iron deficiency-induced chlorosis depends on phosphorus availability. How plants integrate these cues to control chlorophyll accumulation is unknown. Here, we show that iron limitation downregulates photosynthesis genes in a phosphorus-dependent manner. Using transcriptomics and genome-wide association analysis, we identify two genes, PHT4;4 encoding a chloroplastic ascorbate transporter and bZIP58, ...[more]

PMID: 34893639

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Project description:Controlled release phosphorus (P) fertilizers and humic acid (HA) applications are two effective and significant techniques or measures for preventing P loss and enhancing maize development. However, the underlying physiological mechanism of how the controlled release P fertilizers combined with HA affect the maize production and P-use efficiency (PUE) remains unknown. The effects of applying coated diammonium phosphate (CDAP) and HA together on soil nutrient supply intensity, soil phosphatase activity, photosynthesis, endogenous hormone contents, and yield of maize, as well as PUE, were examined in this study. In a pot experiment, two types of P fertilizers-CDAP and diammonium phosphate (DAP)- as well as two HA application rates (0 and 45 kg ha-1) and two P levels (60 and 75 kg P2O5 ha-1) were utilized. Results showed that the key elements that influence the growth and yield of the maize were the availability of P content in soil, plant photosynthesis, and hormone levels. The combination of CDAP and HA had a greater impact on yield and PUE over the course of 2 years than either DAP alone or DAP combined with HA. Besides, using CDAP in combination with HA increased the yield and PUE by 4.2 and 8.4%, respectively, as compared to the application of CDAP alone at 75 kg P2O5 ha-1. From the twelve-leaf to milk stages, the available P content in the soil was increased by an average of 38.6% with the combination of CDAP and HA compared to the application of CDAP alone at 75 kg P2O5 ha-1. In addition, the application of CDAP combined with HA boosted the activities of ATP synthase, as well as the content of cytokinin (CTK), and hence improved the maize photosynthetic rate (Pn). When compared to the application of CDAP alone or DAP combined with HA, the Pn of CDAP + HA treatments was enhanced by 17.9-35.1% at the same P rate. In conclusion, as an environmentally friendly fertilizer, the combined application of CDAP and HA improved the intensity of the soil nutrient supply, regulated photosynthetic capabilities, and increased the yield and PUE, which is important for agricultural production, P resource conservation, and environmental protection.

Project description:BackgroundSoil nutrient status and soil-borne diseases are pivotal factors impacting modern intensive agricultural production. The interplay among plants, soil microbiome, and nutrient regimes in agroecosystems is essential for developing effective disease management. However, the influence of nutrient availability on soil-borne disease suppression and associated plant-microbe interactions remains to be fully explored. T his study aims to elucidate the mechanistic understanding of nutrient impacts on disease suppression, using phosphorous as a target nutrient.ResultsA 6-year field trial involving monocropping of tomatoes with varied fertilizer manipulations demonstrated that phosphorus availability is a key factor driving the control of bacterial wilt disease caused by Ralstonia solanacearum. Subsequent greenhouse experiments were then conducted to delve into the underlying mechanisms of this phenomenon by varying phosphorus availability for tomatoes challenged with the pathogen. Results showed that the alleviation of phosphorus stress promoted the disease-suppressive capacity of the rhizosphere microbiome, but not that of the bulk soil microbiome. This appears to be an extension of the plant trade-off between investment in disease defense mechanisms versus phosphorus acquisition. Adequate phosphorus levels were associated with elevated secretion of root metabolites such as L-tryptophan, methoxyindoleacetic acid, O-phosphorylethanolamine, or mangiferin, increasing the relative density of microbial biocontrol populations such as Chryseobacterium in the rhizosphere. On the other hand, phosphorus deficiency triggered an alternate defense strategy, via root metabolites like blumenol A or quercetin to form symbiosis with arbuscular mycorrhizal fungi, which facilitated phosphorus acquisition as well.ConclusionOverall, our study shows how phosphorus availability can influence the disease suppression capability of the soil microbiome through plant-microbial interactions. These findings highlight the importance of optimizing nutrient regimes to enhance disease suppression, facilitating targeted crop management and boosting agricultural productivity. Video Abstract.

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Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling.

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Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling.

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