Plants

1228 KiB

Open AccessReview

Functional Analysis of Jasmonates in Rice through Mutant Approaches

by Rohit Dhakarey, Preshobha Kodackattumannil Peethambaran and Michael Riemann

Plants 2016, 5(1), 15; https://doi.org/10.3390/plants5010015 - 18 Mar 2016

Cited by 22 | Viewed by 10069

Jasmonic acid, one of the major plant hormones, is, unlike other hormones, a lipid-derived compound that is synthesized from the fatty acid linolenic acid. It has been studied intensively in many plant species including Arabidopsis thaliana, in which most of the enzymes [...] Read more.

Jasmonic acid, one of the major plant hormones, is, unlike other hormones, a lipid-derived compound that is synthesized from the fatty acid linolenic acid. It has been studied intensively in many plant species including Arabidopsis thaliana, in which most of the enzymes participating in its biosynthesis were characterized. In the past 15 years, mutants and transgenic plants affected in the jasmonate pathway became available in rice and facilitate studies on the functions of this hormone in an important crop. Those functions are partially conserved compared to other plant species, and include roles in fertility, response to mechanical wounding and defense against herbivores. However, new and surprising functions have also been uncovered by mutant approaches, such as a close link between light perception and the jasmonate pathway. This was not only useful to show a phenomenon that is unique to rice but also helped to establish this role in plant species where such links are less obvious. This review aims to provide an overview of currently available rice mutants and transgenic plants in the jasmonate pathway and highlights some selected roles of jasmonate in this species, such as photomorphogenesis, and abiotic and biotic stress. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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661 KiB

Open AccessReview

Beyond the Canon: Within-Plant and Population-Level Heterogeneity in Jasmonate Signaling Engaged by Plant-Insect Interactions

by Dapeng Li, Ian T. Baldwin and Emmanuel Gaquerel

Plants 2016, 5(1), 14; https://doi.org/10.3390/plants5010014 - 16 Mar 2016

Cited by 10 | Viewed by 7331

Abstract

Plants have evolved sophisticated communication and defense systems with which they interact with insects. Jasmonates are synthesized from the oxylipin pathway and act as pivotal cellular orchestrators of many of the metabolic and physiological processes that mediate these interactions. Many of these jasmonate-dependent [...] Read more.

Plants have evolved sophisticated communication and defense systems with which they interact with insects. Jasmonates are synthesized from the oxylipin pathway and act as pivotal cellular orchestrators of many of the metabolic and physiological processes that mediate these interactions. Many of these jasmonate-dependent responses are tissue-specific and translate from modulations of the canonical jasmonate signaling pathway. Here we provide a short overview of within-plant heterogeneities in jasmonate signaling and dependent responses in the context of plant-insect interactions as illuminated by examples from recent work with the ecological model, Nicotiana attenuata. We then discuss means of manipulating jasmonate signaling by creating tissue-specific jasmonate sinks, and the micrografting of different transgenic plants. The metabolic phenotyping of these manipulations provides an integrative understanding of the functional significance of deviations from the canonical model of this hormonal pathway. Additionally, natural variation in jasmonate biosynthesis and signaling both among and within species can explain polymorphisms in resistance to insects in nature. In this respect, insect-guided explorations of population-level variations in jasmonate metabolism have revealed more complexity than previously realized and we discuss how different “omic” techniques can be used to exploit the natural variation that occurs in this important signaling pathway. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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2177 KiB

Open AccessArticle

Effect of Drought on Herbivore-Induced Plant Gene Expression: Population Comparison for Range Limit Inferences

by Gunbharpur Singh Gill, Riston Haugen, Steven L. Matzner, Abdelali Barakat and David H. Siemens

Plants 2016, 5(1), 13; https://doi.org/10.3390/plants5010013 - 11 Mar 2016

Cited by 4 | Viewed by 5847

Abstract

Low elevation “trailing edge” range margin populations typically face increases in both abiotic and biotic stressors that may contribute to range limit development. We hypothesize that selection may act on ABA and JA signaling pathways for more stable expression needed for range expansion, [...] Read more.

Low elevation “trailing edge” range margin populations typically face increases in both abiotic and biotic stressors that may contribute to range limit development. We hypothesize that selection may act on ABA and JA signaling pathways for more stable expression needed for range expansion, but that antagonistic crosstalk prevents their simultaneous co-option. To test this hypothesis, we compared high and low elevation populations of Boechera stricta that have diverged with respect to constitutive levels of glucosinolate defenses and root:shoot ratios; neither population has high levels of both traits. If constraints imposed by antagonistic signaling underlie this divergence, one would predict that high constitutive levels of traits would coincide with lower plasticity. To test this prediction, we compared the genetically diverged populations in a double challenge drought-herbivory growth chamber experiment. Although a glucosinolate defense response to the generalist insect herbivore Spodoptera exigua was attenuated under drought conditions, the plastic defense response did not differ significantly between populations. Similarly, although several potential drought tolerance traits were measured, only stomatal aperture behavior, as measured by carbon isotope ratios, was less plastic as predicted in the high elevation population. However, RNAseq results on a small subset of plants indicated differential expression of relevant genes between populations as predicted. We suggest that the ambiguity in our results stems from a weaker link between the pathways and the functional traits compared to transcripts. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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Open AccessArticle

Detection of Leptosphaeria maculans and Leptosphaeria biglobosa Causing Blackleg Disease in Canola from Canadian Canola Seed Lots and Dockage

by W. G. Dilantha Fernando, Xuehua Zhang and Chami C. Amarasinghe

Plants 2016, 5(1), 12; https://doi.org/10.3390/plants5010012 - 1 Mar 2016

Cited by 25 | Viewed by 7662

Abstract

Blackleg, caused by Leptosphaeria maculans, is a major threat to canola production in Canada. With the exception of China, L. maculans is present in areas around the world where cruciferous crops are grown. The pathogen can cause trade barriers in international [...] Read more.

Blackleg, caused by Leptosphaeria maculans, is a major threat to canola production in Canada. With the exception of China, L. maculans is present in areas around the world where cruciferous crops are grown. The pathogen can cause trade barriers in international canola seed export due to its potential risk as a seed contaminant. The most recent example is China restricting canola seeds imported from Canada and Australia in 2009. Therefore, it is important to assess the level of Blackleg infection in Canadian canola seed lots and dockage (seeds and admixture). In this study, canola seed lots and dockage samples collected from Western Canada were tested for the presence of the aggressive L. maculans and the less aggressive L. biglobosa. Results showed that both L. maculans and L. biglobosa were present in seed lots and dockage samples, with L. biglobosa being predominant in infected seeds. Admixture separated from dockage had higher levels of L. maculans and L. biglobosa infection than samples from seed lots. Admixture appears to harbour higher levels of L. maculans infection compared to seeds and is more likely to be a major source of inoculum for the spread of the disease than infected seeds. Full article

(This article belongs to the Special Issue Selected/Extended Full Papers of 14th International Rapeseed Congress)

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509 KiB

Open AccessCommunication

Jasmonate Signalling and Defence Responses in the Model Legume Medicago truncatula—A Focus on Responses to Fusarium Wilt Disease

by Louise F. Thatcher, Ling-Ling Gao and Karam B. Singh

Plants 2016, 5(1), 11; https://doi.org/10.3390/plants5010011 - 5 Feb 2016

Cited by 13 | Viewed by 7046

Abstract

Jasmonate (JA)-mediated defences play important roles in host responses to pathogen attack, in particular to necrotrophic fungal pathogens that kill host cells in order to extract nutrients and live off the dead plant tissue. The root-infecting fungal pathogen Fusarium oxysporum initiates a necrotrophic [...] Read more.

Jasmonate (JA)-mediated defences play important roles in host responses to pathogen attack, in particular to necrotrophic fungal pathogens that kill host cells in order to extract nutrients and live off the dead plant tissue. The root-infecting fungal pathogen Fusarium oxysporum initiates a necrotrophic growth phase towards the later stages of its lifecycle and is responsible for devastating Fusarium wilt disease on numerous legume crops worldwide. Here we describe the use of the model legume Medicago truncatula to study legume–F. oxysporum interactions and compare and contrast this against knowledge from other model pathosystems, in particular Arabidopsis thaliana–F. oxysporum interactions. We describe publically-available genomic, transcriptomic and genetic (mutant) resources developed in M. truncatula that enable dissection of host jasmonate responses and apply aspects of these herein during the M. truncatula-–F. oxysporum interaction. Our initial results suggest not all components of JA-responses observed in M. truncatula are shared with Arabidopsis in response to F. oxysporum infection. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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297 KiB

Open AccessEditorial

Acknowledgement to Reviewers of Plants in 2015

by Plants Editorial Office

Plants 2016, 5(1), 10; https://doi.org/10.3390/plants5010010 - 21 Jan 2016

Viewed by 3429

Abstract

The editors of Plants would like to express their sincere gratitude to the following reviewers for assessing manuscripts in 2015. [...] Full article

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Open AccessReview

How Microbes Twist Jasmonate Signaling around Their Little Fingers

by Selena Gimenez-Ibanez, Andrea Chini and Roberto Solano

Plants 2016, 5(1), 9; https://doi.org/10.3390/plants5010009 - 19 Jan 2016

Cited by 61 | Viewed by 9824

Abstract

Plant immunity relies on a complex network of hormone signaling pathways in which jasmonic acid (JA) plays a central role. Successful microbial pathogens or symbionts have developed strategies to manipulate plant hormone signaling pathways to cause hormonal imbalances for their own benefit. These [...] Read more.

Plant immunity relies on a complex network of hormone signaling pathways in which jasmonic acid (JA) plays a central role. Successful microbial pathogens or symbionts have developed strategies to manipulate plant hormone signaling pathways to cause hormonal imbalances for their own benefit. These strategies include the production of plant hormones, phytohormone mimics, or effector proteins that target host components to disrupt hormonal signaling pathways and enhance virulence. Here, we describe the molecular details of the most recent and best-characterized examples of specific JA hormonal manipulation by microbes, which exemplify the ingenious ways by which pathogens can take control over the plant’s hormone signaling network to suppress host immunity. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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1005 KiB

Open AccessCommunication

The C2 Protein from the Geminivirus Tomato Yellow Leaf Curl Sardinia Virus Decreases Sensitivity to Jasmonates and Suppresses Jasmonate-Mediated Defences

by Tábata Rosas-Díaz, Alberto P. Macho, Carmen R. Beuzón, Rosa Lozano-Durán and Eduardo R. Bejarano

Plants 2016, 5(1), 8; https://doi.org/10.3390/plants5010008 - 15 Jan 2016

Cited by 34 | Viewed by 8258

Abstract

An increasing body of evidence points at a role of the plant hormones jasmonates (JAs) in determining the outcome of plant-virus interactions. Geminiviruses, small DNA viruses infecting a wide range of plant species worldwide, encode a multifunctional protein, C2, which is essential for [...] Read more.

An increasing body of evidence points at a role of the plant hormones jasmonates (JAs) in determining the outcome of plant-virus interactions. Geminiviruses, small DNA viruses infecting a wide range of plant species worldwide, encode a multifunctional protein, C2, which is essential for full pathogenicity. The C2 protein has been shown to suppress the JA response, although the current view on the extent of this effect and the underlying molecular mechanisms is incomplete. In this work, we use a combination of exogenous hormone treatments, microarray analysis, and pathogen infections to analyze, in detail, the suppression of the JA response exerted by C2. Our results indicate that C2 specifically affects certain JA-induced responses, namely defence and secondary metabolism, and show that plants expressing C2 are more susceptible to pathogen attack. We propose a model in which C2 might interfere with the JA response at several levels. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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740 KiB

Open AccessReview

Control of Carbon Assimilation and Partitioning by Jasmonate: An Accounting of Growth–Defense Tradeoffs

by Nathan E. Havko, Ian T. Major, Jeremy B. Jewell, Elham Attaran, John Browse and Gregg A. Howe

Plants 2016, 5(1), 7; https://doi.org/10.3390/plants5010007 - 15 Jan 2016

Cited by 87 | Viewed by 11637

Abstract

Plant growth is often constrained by the limited availability of resources in the microenvironment. Despite the continuous threat of attack from insect herbivores and pathogens, investment in defense represents a lost opportunity to expand photosynthetic capacity in leaves and absorption of nutrients and [...] Read more.

Plant growth is often constrained by the limited availability of resources in the microenvironment. Despite the continuous threat of attack from insect herbivores and pathogens, investment in defense represents a lost opportunity to expand photosynthetic capacity in leaves and absorption of nutrients and water by roots. To mitigate the metabolic expenditure on defense, plants have evolved inducible defense strategies. The plant hormone jasmonate (JA) is a key regulator of many inducible defenses. Synthesis of JA in response to perceived danger leads to the deployment of a variety of defensive structures and compounds, along with a potent inhibition of growth. Genetic studies have established an important role for JA in mediating tradeoffs between growth and defense. However, several gaps remain in understanding of how JA signaling inhibits growth, either through direct transcriptional control of JA-response genes or crosstalk with other signaling pathways. Here, we highlight recent progress in uncovering the role of JA in controlling growth-defense balance and its relationship to resource acquisition and allocation. We also discuss tradeoffs in the context of the ability of JA to promote increased leaf mass per area (LMA), which is a key indicator of leaf construction costs and leaf life span. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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Graphical abstract

1568 KiB

Open AccessReview

The Ubiquitin System and Jasmonate Signaling

by Astrid Nagels Durand, Laurens Pauwels and Alain Goossens

Plants 2016, 5(1), 6; https://doi.org/10.3390/plants5010006 - 9 Jan 2016

Cited by 40 | Viewed by 10003

Abstract

The ubiquitin (Ub) system is involved in most, if not all, biological processes in eukaryotes. The major specificity determinants of this system are the E3 ligases, which bind and ubiquitinate specific sets of proteins and are thereby responsible for target recruitment to the [...] Read more.

The ubiquitin (Ub) system is involved in most, if not all, biological processes in eukaryotes. The major specificity determinants of this system are the E3 ligases, which bind and ubiquitinate specific sets of proteins and are thereby responsible for target recruitment to the proteasome or other cellular processing machineries. The Ub system contributes to the regulation of the production, perception and signal transduction of plant hormones. Jasmonic acid (JA) and its derivatives, known as jasmonates (JAs), act as signaling compounds regulating plant development and plant responses to various biotic and abiotic stress conditions. We provide here an overview of the current understanding of the Ub system involved in JA signaling. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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1382 KiB

Open AccessArticle

Defense Priming and Jasmonates: A Role for Free Fatty Acids in Insect Elicitor-Induced Long Distance Signaling

by Ting Li, Tristan Cofer, Marie Engelberth and Jurgen Engelberth

Plants 2016, 5(1), 5; https://doi.org/10.3390/plants5010005 - 8 Jan 2016

Cited by 20 | Viewed by 7459

Abstract

Green leaf volatiles (GLV) prime plants against insect herbivore attack resulting in stronger and faster signaling by jasmonic acid (JA). In maize this response is specifically linked to insect elicitor (IE)-induced signaling processes, which cause JA accumulation not only around the damage site, [...] Read more.

Green leaf volatiles (GLV) prime plants against insect herbivore attack resulting in stronger and faster signaling by jasmonic acid (JA). In maize this response is specifically linked to insect elicitor (IE)-induced signaling processes, which cause JA accumulation not only around the damage site, but also in distant tissues, presumably through the activation of electrical signals. Here, we present additional data further characterizing these distal signaling events in maize. Also, we describe how exposure to GLV increases free fatty acid (fFA) levels in maize seedlings, but also in other plants, and how increased fFA levels affect IE-induced JA accumulation. Increased fFA, in particular α-linolenic acid (LnA), caused a significant increase in JA accumulation after IE treatment, while JA induced by mechanical wounding (MW) alone was not affected. We also identified treatments that significantly decreased certain fFA level including simulated wind and rain. In such treated plants, IE-induced JA accumulation was significantly reduced when compared to un-moved control plants, while MW-induced JA accumulation was not significantly affected. Since only IE-induced JA accumulation was altered by changes in the fFA composition, we conclude that changing levels of fFA affect primarily IE-induced signaling processes rather than serving as a substrate for JA. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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Open AccessArticle

Dynamics of Jasmonate Metabolism upon Flowering and across Leaf Stress Responses in Arabidopsis thaliana

by Emilie Widemann, Ekaterina Smirnova, Yann Aubert, Laurence Miesch and Thierry Heitz

Plants 2016, 5(1), 4; https://doi.org/10.3390/plants5010004 - 6 Jan 2016

Cited by 28 | Viewed by 7564

Abstract

The jasmonic acid (JA) signaling pathway plays important roles in adaptation of plants to environmental cues and in specific steps of their development, particularly in reproduction. Recent advances in metabolic studies have highlighted intricate mechanisms that govern enzymatic conversions within the jasmonate family. [...] Read more.

The jasmonic acid (JA) signaling pathway plays important roles in adaptation of plants to environmental cues and in specific steps of their development, particularly in reproduction. Recent advances in metabolic studies have highlighted intricate mechanisms that govern enzymatic conversions within the jasmonate family. Here we analyzed jasmonate profile changes upon Arabidopsis thaliana flower development and investigated the contribution of catabolic pathways that were known to turnover the active hormonal compound jasmonoyl-isoleucine (JA-Ile) upon leaf stress. We report a rapid decline of JA-Ile upon flower opening, concomitant with the massive accumulation of its most oxidized catabolite, 12COOH-JA-Ile. Detailed genetic analysis identified CYP94C1 as the major player in this process. CYP94C1 is one out of three characterized cytochrome P450 enzymes that define an oxidative JA-Ile turnover pathway, besides a second, hydrolytic pathway represented by the amido-hydrolases IAR3 and ILL6. Expression studies combined with reporter gene analysis revealed the dominant expression of CYP94C1 in mature anthers, consistent with the established role of JA signaling in male fertility. Significant CYP94B1 expression was also evidenced in stamen filaments, but surprisingly, CYP94B1 deficiency was not associated with significant changes in JA profiles. Finally, we compared global flower JA profiles with those previously reported in leaves reacting to mechanical wounding or submitted to infection by the necrotrophic fungus Botrytis cinerea. These comparisons revealed distinct dynamics of JA accumulation and conversions in these three biological systems. Leaf injury boosts a strong and transient JA and JA-Ile accumulation that evolves rapidly into a profile dominated by ω-oxidized and/or Ile-conjugated derivatives. In contrast, B. cinerea-infected leaves contain mostly unconjugated jasmonates, about half of this content being ω-oxidized. Finally, developing flowers present an intermediate situation where young flower buds show detectable jasmonate oxidation (probably originating from stamen metabolism) which becomes exacerbated upon flower opening. Our data illustrate that in spite conserved enzymatic routes, the jasmonate metabolic grid shows considerable flexibility and dynamically equilibrates into specific blends in different physiological situations. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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1965 KiB

Open AccessFeature PaperArticle

Activity Regulation by Heteromerization of Arabidopsis Allene Oxide Cyclase Family Members

by Markus Otto, Christin Naumann, Wolfgang Brandt, Claus Wasternack and Bettina Hause

Plants 2016, 5(1), 3; https://doi.org/10.3390/plants5010003 - 6 Jan 2016

Cited by 25 | Viewed by 8038

Abstract

Jasmonates (JAs) are lipid-derived signals in plant stress responses and development. A crucial step in JA biosynthesis is catalyzed by allene oxide cyclase (AOC). Four genes encoding functional AOCs (AOC1, AOC2, AOC3 and AOC4) have been characterized for Arabidopsis thaliana in terms of [...] Read more.

Jasmonates (JAs) are lipid-derived signals in plant stress responses and development. A crucial step in JA biosynthesis is catalyzed by allene oxide cyclase (AOC). Four genes encoding functional AOCs (AOC1, AOC2, AOC3 and AOC4) have been characterized for Arabidopsis thaliana in terms of organ- and tissue-specific expression, mutant phenotypes, promoter activities and initial in vivo protein interaction studies suggesting functional redundancy and diversification, including first hints at enzyme activity control by protein-protein interaction. Here, these analyses were extended by detailed analysis of recombinant proteins produced in Escherichia coli. Treatment of purified AOC2 with SDS at different temperatures, chemical cross-linking experiments and protein structure analysis by molecular modelling approaches were performed. Several salt bridges between monomers and a hydrophobic core within the AOC2 trimer were identified and functionally proven by site-directed mutagenesis. The data obtained showed that AOC2 acts as a trimer. Finally, AOC activity was determined in heteromers formed by pairwise combinations of the four AOC isoforms. The highest activities were found for heteromers containing AOC4 + AOC1 and AOC4 + AOC2, respectively. All data are in line with an enzyme activity control of all four AOCs by heteromerization, thereby supporting a putative fine-tuning in JA formation by various regulatory principles. Full article

(This article belongs to the Special Issue The Jasmonate Pathway)

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2479 KiB

Open AccessArticle

Response of Arabidopsis thaliana Roots with Altered Lipid Transfer Protein (LTP) Gene Expression to the Clubroot Disease and Salt Stress

by Sabine Jülke and Jutta Ludwig-Müller

Plants 2016, 5(1), 2; https://doi.org/10.3390/plants5010002 - 24 Dec 2015

Cited by 34 | Viewed by 9376

Abstract

The clubroot disease of Brassicaceae is caused by the obligate biotrophic protist Plasmodiophora brassicae. The disease is characterized by abnormal tumorous swellings of infected roots that result in reduced drought resistance and insufficient distribution of nutrients, leading to reduced crop yield. It [...] Read more.

The clubroot disease of Brassicaceae is caused by the obligate biotrophic protist Plasmodiophora brassicae. The disease is characterized by abnormal tumorous swellings of infected roots that result in reduced drought resistance and insufficient distribution of nutrients, leading to reduced crop yield. It is one of the most damaging diseases among cruciferous crops worldwide. The acquisition of nutrients by the protist is not well understood. Gene expression profiles in Arabidopsis thaliana clubroots indicate that lipid transfer proteins (LTPs) could be involved in disease development or at least in adaptation to the disease symptoms. Therefore, the aim of the study was to examine the role of some, of the still enigmatic LTPs during clubroot development. For a functional approach, we have generated transgenic plants that overexpress LTP genes in a root specific manner or show reduced LTP gene expression. Our results showed that overexpression of some of the LTP genes resulted in reduced disease severity whereas the lipid content in clubs of LTP mutants seems to be unaffected. Additional studies indicate a role for some LTPs during salt stress conditions in roots of A. thaliana. Full article

(This article belongs to the Special Issue Plant Root Development)

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1783 KiB

Open AccessArticle

A Comparative Study of Proteolytic Mechanisms during Leaf Senescence of Four Genotypes of Winter Oilseed Rape Highlighted Relevant Physiological and Molecular Traits for NRE Improvement

by Alexandra Girondé, Marine Poret, Philippe Etienne, Jacques Trouverie, Alain Bouchereau, Françoise Le Cahérec, Laurent Leport, Marie-Françoise Niogret and Jean-Christophe Avice

Plants 2016, 5(1), 1; https://doi.org/10.3390/plants5010001 - 22 Dec 2015

Cited by 10 | Viewed by 6164

Abstract

Winter oilseed rape is characterized by a low N use efficiency related to a weak leaf N remobilization efficiency (NRE) at vegetative stages. By investigating the natural genotypic variability of leaf NRE, our goal was to characterize the relevant physiological traits and the [...] Read more.

Winter oilseed rape is characterized by a low N use efficiency related to a weak leaf N remobilization efficiency (NRE) at vegetative stages. By investigating the natural genotypic variability of leaf NRE, our goal was to characterize the relevant physiological traits and the main protease classes associated with an efficient proteolysis and high leaf NRE in response to ample or restricted nitrate supply. The degradation rate of soluble proteins and D1 protein (a thylakoid-bound protein) were correlated to N remobilization, except for the genotype Samouraï which showed a low NRE despite high levels of proteolysis. Under restricted nitrate conditions, high levels of soluble protein degradation were associated with serine, cysteine and aspartic proteases at acidic pH. Low leaf NRE was related to a weak proteolysis of both soluble and thylakoid-bound proteins. The results obtained on the genotype Samouraï suggest that the timing between the onset of proteolysis and abscission could be a determinant. The specific involvement of acidic proteases suggests that autophagy and/or senescence-associated vacuoles are implicated in N remobilization under low N conditions. The data revealed that the rate of D1 degradation could be a relevant indicator of leaf NRE and might be used as a tool for plant breeding. Full article

(This article belongs to the Special Issue Plant Senescence)

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