Root-Derived Proteases as a Plant Tool to Access Soil Organic Nitrogen; Current Stage of Knowledge and Controversies

Adamczyk, Bartosz

doi:10.3390/plants10040731

Cited by 8 publications

(3 citation statements)

References 71 publications

(105 reference statements)

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“…Interactions of plants with the soil environment can be crucially influenced by plant root exudates. For example, plant root exudates can contain primary metabolites to mobilize metals, secondary metabolites to alter microbial microbial composition (17) and proteins for defense or for nutrient scavenging (18) and are therefore a rich source to study interactions of plants and soil environment. One widespread strategy to deal with many types of metal deficiency and toxicity involves secretion of metal-chelating compounds like nicotianamine (19, 20).…”

Section: Introductionmentioning

confidence: 99%

Zinc-starved Brassicaceae Plants Secrete Peptides that Induce Root Expansion

Niehs,

Rajniak,

Johnson

et al. 2024

Preprint

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Zinc (Zn) deficiency is recognized as a global crisis as it is observed in half of all agricultural soils. However, the molecular mechanisms that drive plant physiological responses to soil Zn deficiency are not well understood. We used an untargeted metabolomics approach to search for metabolites exuded from roots during Zn deficiency stress, which led to the discovery of a collection of secreted small defensin-like peptides inArabidopsis thaliana(named Zinc-Deficiency Responsive Peptides (ZDRPs)). Phylogenetic analysis and untargeted metabolomics revealed ZDRPs in at least eleven accessions ofA. thalianaand nine members of the Brassicaceae family. Analysis ofArabidopsisgene mutants and overexpressing lines, in combination with chemical complementation experiments, unveiled a critical role of these peptides in plant root growth. We hypothesize that Brassicaceae secreted peptides enable plants to expand their root mass to reach Zn-rich soil layers and optimize Zn uptake. These data reveal a critical relationship between plant survival, Zn status, root morphology and peptide production. Taken together, our results expand our knowledge regarding micronutrient deficiency responses in plants and could enable in engineering approaches to make plants more resilient to low Zn conditions.SignificanceZinc deficiency is the most abundant micronutrient deficiency affecting about 50% of arable lands thus presenting a high burden for plant health and agriculture globally. In this study, we reveal a metabolic strategy by Brassicaceae to deal with low Zn concentrations. We characterize the role of peptides expressed upon zinc deficiency in a variety of important crop plants. The discovery of a cryptic class of peptides that are made by plant roots specifically suffering from Zn deficiency provides critical insight into the molecular mechanisms by which plants dynamically acclimate to nutrient-limited soils. The identification of peptides actively secreted by zinc-deprived plants has translational value for sustainable agriculture, human health, and bioengineering approaches to enable tolerance to low zinc.

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Section: Introductionmentioning

confidence: 99%

Zinc-starved Brassicaceae Plants Secrete Peptides that Induce Root Expansion

Niehs,

Rajniak,

Johnson

et al. 2024

Preprint

View full text Add to dashboard Cite

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“…Plants produce many proteases that cleave multiple substrates and act in various processes (including development, homeostasis, growth, symbiosis and especially in plant defense and disease resistance), and their activity is tightly regulated accordingly (Godson & van der Hoorn, 2021; van der Hoorn & Klemencic, 2021). Similarly, during organic N uptake, proteases may act through four routes: (1) proteases are released from the roots to the external medium, and the resulting products diffuse back, (2) proteases inside root cells cleave their substrates after protein endocytosis, and (3) proteolysis occurs in root surface cells (with cell wall‐bound proteases) or (4) in the apoplast, to which proteins diffuse through pores (with plasma membrane or inward‐facing cell wall proteases) (Adamczyk, 2021; Greenfield et al, 2020; Kohli et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…(2) proteases inside root cells cleave their substrates after protein endocytosis, and (3) proteolysis occurs in root surface cells (with cell wallbound proteases) or (4) in the apoplast, to which proteins diffuse through pores (with plasma membrane or inward-facing cell wall proteases) (Adamczyk, 2021;Greenfield et al, 2020;Kohli et al, 2012).…”

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confidence: 99%

Casein as protein and hydrolysate: Biostimulant or nitrogen source for Nicotiana tabacum plants grown in vitro?

Bělonožníková

Černý

Hýsková

et al. 2023

Physiologia Plantarum

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In contrast to inorganic nitrogen (N) assimilation, the role of organic N forms, such as proteins and peptides, as sources of N and their impact on plant metabolism remains unclear. Simultaneously, organic biostimulants are used as priming agents to improve plant defense response. Here, we analysed the metabolic response of tobacco plants grown in vitro with casein hydrolysate or protein. As the sole source of N, casein hydrolysate enabled tobacco growth, while protein casein was used only to a limited extent. Free amino acids were detected in the roots of tobacco plants grown with protein casein but not in the plants grown with no source of N. Combining hydrolysate with inorganic N had beneficial effects on growth, root N uptake and protein content. The metabolism of casein‐supplemented plants shifted to aromatic (Trp), branched‐chain (Ile, Leu, Val) and basic (Arg, His, Lys) amino acids, suggesting their preferential uptake and/or alterations in their metabolic pathways. Complementarily, proteomic analysis of tobacco roots identified peptidase C1A and peptidase S10 families as potential key players in casein degradation and response to N starvation. Moreover, amidases were significantly upregulated, most likely for their role in ammonia release and impact on auxin synthesis. In phytohormonal analysis, both forms of casein influenced phenylacetic acid and cytokinin contents, suggesting a root system response to scarce N availability. In turn, metabolomics highlighted the stimulation of some plant defense mechanisms under such growth conditions, that is, the high concentrations of secondary metabolites (e.g., ferulic acid) and heat shock proteins.

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How to get to the N – a call for interdisciplinary research on organic N utilization pathways by plants

Holz,

Lewin,

Kolb

et al. 2024

Plant Soil

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Background and aims While nitrogen (N) derived from soil organic matter significantly sustains agricultural plants, the complexities of organic N utilization pathways remain poorly understood. Knowledge gaps persist regarding diverse organic N pools, the microbial processes in N mineralization, and how plants shape the N-mineralizing microbial community through root exudation. Results To address these gaps, we propose an integrated conceptual framework that explores the intricate interplay of soil, plant, and microbiome dynamics within the context of soil carbon (C) cycling. Emphasizing plant effects on gross depolymerization and deamination of organic N—a crucial yet often overlooked aspect—we aim to enhance our understanding of plant N utilization pathways. In this context, we suggest considering the linkages between root and hyphal exudation, followed by rhizosphere priming effects which in turn control N mobilization. Based on the relation between exudation and N turnover, we identify microbial necromass as a potentially important organic N source for plants. Furthermore, we propose applying root economic theory to gain insights into the diverse strategies employed by plants in accessing soil organic N. Stable isotope tracers and functional microbiome analytics provide tools to decipher the complex network of the pathways of organic N utilization. Conclusions The envisioned holistic framework for organic N utilization pathways, intricately connects plants, soil, and microorganisms. This lays the groundwork for sustainable agricultural practices, potentially reducing N losses.

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Root-Derived Proteases as a Plant Tool to Access Soil Organic Nitrogen; Current Stage of Knowledge and Controversies

Cited by 8 publications

References 71 publications

Zinc-starved Brassicaceae Plants Secrete Peptides that Induce Root Expansion

Zinc-starved Brassicaceae Plants Secrete Peptides that Induce Root Expansion

Casein as protein and hydrolysate: Biostimulant or nitrogen source for Nicotiana tabacum plants grown in vitro?

How to get to the N – a call for interdisciplinary research on organic N utilization pathways by plants

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