Cells

Research

14 pages, 5715 KiB

Open AccessFeature PaperArticle

A New Player in Jasmonate-Mediated Stomatal Closure: The Arabidopsis thaliana Copper Amine Oxidase β

by Ilaria Fraudentali, Chiara Pedalino, Paraskevi Tavladoraki, Riccardo Angelini and Alessandra Cona

Cells 2021, 10(12), 3399; https://doi.org/10.3390/cells10123399 - 2 Dec 2021

Cited by 5 | Viewed by 2453

Abstract

Plant defence responses to adverse environmental conditions include different stress signalling, allowing plant acclimation and survival. Among these responses one of the most common, immediate, and effective is the modulation of the stomatal aperture, which integrates different transduction pathways involving hydrogen peroxide (H [...] Read more.

Plant defence responses to adverse environmental conditions include different stress signalling, allowing plant acclimation and survival. Among these responses one of the most common, immediate, and effective is the modulation of the stomatal aperture, which integrates different transduction pathways involving hydrogen peroxide (H₂O₂), calcium (Ca²⁺), nitric oxide (NO), phytohormones and other signalling components. The Arabidopsis thaliana copper amine oxidases β (AtCuAOβ) encodes an apoplastic CuAO expressed in guard cells and root protoxylem tissues which oxidizes polyamines to aminoaldehydes with the production of H₂O₂ and ammonia. Here, its role in stomatal closure, signalled by the wound-associated phytohormone methyl-jasmonate (MeJA) was explored by pharmacological and genetic approaches. Obtained data show that AtCuAOβ tissue-specific expression is induced by MeJA, especially in stomata guard cells. Interestingly, two Atcuaoβ T-DNA insertional mutants are unresponsive to this hormone, showing a compromised MeJA-mediated stomatal closure compared to the wild-type (WT) plants. Coherently, Atcuaoβ mutants also show compromised H₂O₂-production in guard cells upon MeJA treatment. Furthermore, the H₂O₂ scavenger N,N¹-dimethylthiourea (DMTU) and the CuAO-specific inhibitor 2-bromoethylamine (2-BrEtA) both reversed the MeJA-induced stomatal closure and the H₂O₂ production in WT plants. Our data suggest that AtCuAOβ is involved in the H₂O₂ production implicated in MeJA-induced stomatal closure. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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10 pages, 824 KiB

Open AccessArticle

Responses of Polyamine-Metabolic Genes to Polyamines and Plant Stress Hormones in Arabidopsis Seedlings

by Yusaku Yariuchi, Takashi Okamoto, Yoshiteru Noutoshi and Taku Takahashi

Cells 2021, 10(12), 3283; https://doi.org/10.3390/cells10123283 - 24 Nov 2021

Cited by 13 | Viewed by 3075

Abstract

In plants, many of the enzymes in polyamine metabolism are encoded by multiple genes, whose expressions are differentially regulated under different physiological conditions. For comprehensive understanding of their regulation during the seedling growth stage, we examined the expression of polyamine metabolic genes in [...] Read more.

In plants, many of the enzymes in polyamine metabolism are encoded by multiple genes, whose expressions are differentially regulated under different physiological conditions. For comprehensive understanding of their regulation during the seedling growth stage, we examined the expression of polyamine metabolic genes in response to polyamines and stress-related plant hormones in Arabidopsis thaliana. While confirming previous findings such as induction of many of the genes by abscisic acid, induction of arginase genes and a copper amine oxidase gene, CuAOα3, by methyl jasmonate, that of an arginine decarboxylase gene, ADC2, and a spermine synthase gene, SPMS, by salicylic acid, and negative feedback regulation of thermospermine biosynthetic genes by thermospermine, our results showed that expressions of most of the genes are not responsive to exogenous polyamines. We thus examined expression of OsPAO6, which encodes an apoplastic polyamine oxidase and is strongly induced by polyamines in rice, by using the promoter-GUS fusion in transgenic Arabidopsis seedlings. The GUS activity was increased by treatment with methyl jasmonate but neither by polyamines nor by other plant hormones, suggesting a difference in the response to polyamines between Arabidopsis and rice. Our results provide a framework to study regulatory modules directing expression of each polyamine metabolic gene. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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15 pages, 13344 KiB

Open AccessArticle

Polyamine Metabolism in Scots Pine Embryogenic Cells under Potassium Deficiency

by Riina Muilu-Mäkelä, Jaana Vuosku, Hely Häggman and Tytti Sarjala

Cells 2021, 10(5), 1244; https://doi.org/10.3390/cells10051244 - 18 May 2021

Cited by 2 | Viewed by 2629

Abstract

Polyamines (PA) have a protective role in maintaining growth and development in Scots pine during abiotic stresses. In the present study, a controlled liquid Scots pine embryogenic cell culture was used for studying the responses of PA metabolism related to potassium deficiency. The [...] Read more.

Polyamines (PA) have a protective role in maintaining growth and development in Scots pine during abiotic stresses. In the present study, a controlled liquid Scots pine embryogenic cell culture was used for studying the responses of PA metabolism related to potassium deficiency. The transcription level regulation of PA metabolism led to the accumulation of putrescine (Put). Arginine decarboxylase (ADC) had an increased expression trend under potassium deficiency, whereas spermidine synthase (SPDS) expression decreased. Generally, free spermidine (Spd) and spermine (Spm)/ thermospermine (t-Spm) contents were kept relatively stable, mostly by the downregulation of polyamine oxidase (PAO) expression. The low potassium contents in the culture medium decreased the potassium content of the cells, which inhibited cell mass growth, but did not affect cell viability. The reduced growth was probably caused by repressed metabolic activity and cell division, whereas there were no signs of H₂O₂-induced oxidative stress or increased cell death. The low intracellular content of K⁺ decreased the content of Na⁺. The decrease in the pH of the culture medium indicated that H⁺ ions were pumped out of the cells. Altogether, our findings emphasize the specific role(s) of Put under potassium deficiency and strict developmental regulation of PA metabolism in Scots pine. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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19 pages, 3416 KiB

Open AccessArticle

Polyamines and Their Biosynthesis/Catabolism Genes Are Differentially Modulated in Response to Heat Versus Cold Stress in Tomato Leaves (Solanum lycopersicum L.)

by Rakesh K. Upadhyay, Tahira Fatima, Avtar K. Handa and Autar K. Mattoo

Cells 2020, 9(8), 1749; https://doi.org/10.3390/cells9081749 - 22 Jul 2020

Cited by 36 | Viewed by 4734

Abstract

Polyamines (PAs) regulate growth in plants and modulate the whole plant life cycle. They have been associated with different abiotic and biotic stresses, but little is known about the molecular regulation involved. We quantified gene expression of PA anabolic and catabolic pathway enzymes [...] Read more.

Polyamines (PAs) regulate growth in plants and modulate the whole plant life cycle. They have been associated with different abiotic and biotic stresses, but little is known about the molecular regulation involved. We quantified gene expression of PA anabolic and catabolic pathway enzymes in tomato (Solanum lycopersicum cv. Ailsa Craig) leaves under heat versus cold stress. These include arginase 1 and 2, arginine decarboxylase 1 and 2, agmatine iminohydrolase/deiminase 1, N-carbamoyl putrescine amidase, two ornithine decarboxylases, three S-adenosylmethionine decarboxylases, two spermidine synthases; spermine synthase; flavin-dependent polyamine oxidases (SlPAO4-like and SlPAO2) and copper dependent amine oxidases (SlCuAO and SlCuAO-like). The spatiotemporal transcript abundances using qRT-PCR revealed presence of their transcripts in all tissues examined, with higher transcript levels observed for SAMDC1, SAMDC2 and ADC2 in most tissues. Cellular levels of free and conjugated forms of putrescine and spermidine were found to decline during heat stress while they increased in response to cold stress, revealing their differential responses. Transcript levels of ARG2, SPDS2, and PAO4-like increased in response to both heat and cold stresses. However, transcript levels of ARG1/2, AIH1, CPA, SPDS1 and CuAO4 increased in response to heat while those of ARG2, ADC1,2, ODC1, SAMDC1,2,3, PAO2 and CuPAO4-like increased in response to cold stress, respectively. Transcripts of ADC1,2, ODC1,2, and SPMS declined in response to heat stress while ODC2 transcripts declined under cold stress. These results show differential expression of PA metabolism genes under heat and cold stresses with more impairment clearly seen under heat stress. We interpret these results to indicate a more pronounced role of PAs in cold stress acclimation compared to that under heat stress in tomato leaves. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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25 pages, 3871 KiB

Open AccessArticle

The Barley S-Adenosylmethionine Synthetase 3 Gene HvSAMS3 Positively Regulates the Tolerance to Combined Drought and Salinity Stress in Tibetan Wild Barley

by Imrul Mosaddek Ahmed, Umme Aktari Nadira, Cheng-Wei Qiu, Fangbin Cao, Zhong-Hua Chen, Eva Vincze and Feibo Wu

Cells 2020, 9(6), 1530; https://doi.org/10.3390/cells9061530 - 23 Jun 2020

Cited by 26 | Viewed by 4239 | Correction

Abstract

Drought and salinity are two of the most frequently co-occurring abiotic stresses. Despite recent advances in the elucidation of the effects of these stresses individually during the vegetative stage of plants, significant gaps exist in our understanding of the combined effects of these [...] Read more.

Drought and salinity are two of the most frequently co-occurring abiotic stresses. Despite recent advances in the elucidation of the effects of these stresses individually during the vegetative stage of plants, significant gaps exist in our understanding of the combined effects of these two frequently co-occurring stresses. Here, Tibetan wild barley XZ5 (drought tolerant), XZ16 (salt tolerant), and cultivated barley cv. CM72 (salt tolerant) were subjected to drought (D), salinity (S), or a combination of both treatments (D+S). Protein synthesis is one of the primary activities of the green part of the plant. Therefore, leaf tissue is an important parameter to evaluate drought and salinity stress conditions. Sixty differentially expressed proteins were identified by mass spectrometry (MALDI-TOF/TOF) and classified into 9 biological processes based on Gene Ontology annotation. Among them, 21 proteins were found to be expressed under drought or salinity alone; however, under D+S, 7 proteins, including S-adenosylmethionine synthetase 3 (SAMS3), were exclusively upregulated in drought-tolerant XZ5 but not in CM72. HvSAMS3 carries both N-terminal and central domains compared with Arabidopsis and activates the expression of several ethylene (ET)-responsive transcription factors. HvSAMS3 is mainly expressed in the roots and stems, and HvSAMS3 is a secretory protein located in the cell membrane and cytoplasm. Barley stripe mosaic virus-based virus-induced gene silencing (BSMV-VIGS) of HvSAMS3 in XZ5 severely compromised its tolerance to D+S and significantly reduced plant growth and K⁺ uptake. The reduced tolerance to the combined stress was associated with the inhibition of polyamines such as spermidine and spermine, polyamine oxidase, ethylene, biotin, and antioxidant enzyme activities. Furthermore, the exogenous application of ethylene and biotin improved the tolerance to D+S in BSMV-VIGS:HvSAMS3-inoculated plants. Our findings highlight the significance of HvSAMS3 in the tolerance to D+S in XZ5. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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Review

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15 pages, 2115 KiB

Open AccessEditor’s ChoiceReview

Spermine: Its Emerging Role in Regulating Drought Stress Responses in Plants

by Md. Mahadi Hasan, Milan Skalicky, Mohammad Shah Jahan, Md. Nazmul Hossain, Zunaira Anwar, Zheng-Fei Nie, Nadiyah M. Alabdallah, Marian Brestic, Vaclav Hejnak and Xiang-Wen Fang

Cells 2021, 10(2), 261; https://doi.org/10.3390/cells10020261 - 28 Jan 2021

Cited by 102 | Viewed by 8930

Abstract

In recent years, research on spermine (Spm) has turned up a lot of new information about this essential polyamine, especially as it is able to counteract damage from abiotic stresses. Spm has been shown to protect plants from a variety of environmental insults, [...] Read more.

In recent years, research on spermine (Spm) has turned up a lot of new information about this essential polyamine, especially as it is able to counteract damage from abiotic stresses. Spm has been shown to protect plants from a variety of environmental insults, but whether it can prevent the adverse effects of drought has not yet been reported. Drought stress increases endogenous Spm in plants and exogenous application of Spm improves the plants’ ability to tolerate drought stress. Spm’s role in enhancing antioxidant defense mechanisms, glyoxalase systems, methylglyoxal (MG) detoxification, and creating tolerance for drought-induced oxidative stress is well documented in plants. However, the influences of enzyme activity and osmoregulation on Spm biosynthesis and metabolism are variable. Spm interacts with other molecules like nitric oxide (NO) and phytohormones such as abscisic acid, salicylic acid, brassinosteroids, and ethylene, to coordinate the reactions necessary for developing drought tolerance. This review focuses on the role of Spm in plants under severe drought stress. We have proposed models to explain how Spm interacts with existing defense mechanisms in plants to improve drought tolerance. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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20 pages, 1261 KiB

Open AccessFeature PaperEditor’s ChoiceReview

Polyamines: Small Amines with Large Effects on Plant Abiotic Stress Tolerance

by Rubén Alcázar, Milagros Bueno and Antonio F. Tiburcio

Cells 2020, 9(11), 2373; https://doi.org/10.3390/cells9112373 - 29 Oct 2020

Cited by 155 | Viewed by 8631

Abstract

In recent years, climate change has altered many ecosystems due to a combination of frequent droughts, irregular precipitation, increasingly salinized areas and high temperatures. These environmental changes have also caused a decline in crop yield worldwide. Therefore, there is an urgent need to [...] Read more.

In recent years, climate change has altered many ecosystems due to a combination of frequent droughts, irregular precipitation, increasingly salinized areas and high temperatures. These environmental changes have also caused a decline in crop yield worldwide. Therefore, there is an urgent need to fully understand the plant responses to abiotic stress and to apply the acquired knowledge to improve stress tolerance in crop plants. The accumulation of polyamines (PAs) in response to many abiotic stresses is one of the most remarkable plant metabolic responses. In this review, we provide an update about the most significant achievements improving plant tolerance to drought, salinity, low and high temperature stresses by exogenous application of PAs or genetic manipulation of endogenous PA levels. We also provide some clues about possible mechanisms underlying PA functions, as well as known cross-talks with other stress signaling pathways. Finally, we discuss about the possible use of PAs for seed priming to induce abiotic stress tolerance in agricultural valuable crop plants. Full article

(This article belongs to the Special Issue Plant Polyamines in Plant Stress Tolerance)

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