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Molecular Mechanisms of Leaf Senescence

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (10 November 2021) | Viewed by 32603

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Special Issue Editor

Dr. Yasuhito Sakuraba

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Guest Editor

Biotechnology Research Center, The University of Tokyo, Japan
Interests: leaf senescence; plant nutrition; light signaling

Special Issue Information

Dear Colleagues,

Leaf senescence defines the last stage of leaf developmental programs which, when accompanied with extensive destabilization of intracellular organelles and decomposition of macromolecules, works to relocate nutrients to actively developing organs. Since the engineering and breeding of crops with altered onset of leaf senescence could lead to increase crop production and food quality, understanding of molecular mechanisms underlying leaf senescence is important.

In the past couple of decades, massive progress has been made in understanding the regulatory mechanism of leaf senescence, revealing that leaf senescence is an extremely complex genetic program that is controlled by internal factors, including the levels of phytohormones, sugar, and other metabolites, and unfavorable environmental stresses, including light deprivation, drought, high salinity, extreme temperature, nutrient deficiency, and pathogen attacks. However, many molecular mechanisms and associated factors underlying leaf senescence might be still unknown due to its complexity.

The Special Issue is focused on "molecular mechanisms of leaf senescence." We aim to include papers dealing with regulation of leaf senescence at all levels (genes, RNAs, proteins and metabolites), in both model and crop plants.

Dr. Yasuhito Sakuraba
Guest Editor

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Published Papers (11 papers)

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Research

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15 pages, 3588 KiB

Open AccessArticle

Identification and Functional Analysis of Key Autophosphorylation Residues of Arabidopsis Senescence Associated Receptor-like Kinase

by Zhaoxia Guo, Yuanyuan Mei, Dan Wang, Dong Xiao, Xianglin Tang, Yaru Gong, Xinxin Xu and Ning Ning Wang

Int. J. Mol. Sci. 2022, 23(16), 8873; https://doi.org/10.3390/ijms23168873 - 09 Aug 2022

Viewed by 1382

Abstract

Reversible protein phosphorylation mediated by protein kinases and phosphatases plays important roles in the regulation of leaf senescence. We previously reported that the senescence-associated leucine-rich repeat receptor-like kinase AtSARK autophosphorylates on both serine/threonine and tyrosine residues and functions as a positive regulator of Arabidopsis leaf senescence; the senescence-suppressed protein phosphatase SSPP interacts with and dephosphorylates the cytoplasmic domain of AtSARK, thereby negatively regulating leaf senescence. Here, 27 autophosphorylation residues of AtSARK were revealed by mass spectrometry analysis, and six of them, including two Ser, two Thr, and two Tyr residues, were further found to be important for the biological functions of AtSARK. All site-directed mutations of these six residues that resulted in decreased autophosphorylation level of AtSARK could significantly inhibit AtSARK-induced leaf senescence. In addition, mutations mimicking the dephosphorylation form of Ser384 (S384A) or the phosphorylation form of Tyr413 (Y413E) substantially reduced the interaction between AtSARK and SSPP. All results suggest that autophosphorylation of AtSARK is essential for its functions in promoting leaf senescence. The possible roles of S384 and Y413 residues in fine-tuning the interaction between AtSARK and SSPP are discussed herein. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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14 pages, 1246 KiB

Open AccessArticle

Changes in Polar Metabolites Content during Natural and Methyl-Jasmonate-Promoted Senescence of Ginkgo biloba Leaves

by Marcin Horbowicz, Joanna Szablińska-Piernik, Justyna Góraj-Koniarska, Kensuke Miyamoto, Junichi Ueda and Marian Saniewski

Int. J. Mol. Sci. 2022, 23(1), 266; https://doi.org/10.3390/ijms23010266 - 27 Dec 2021

Cited by 6 | Viewed by 2279

Abstract

The present study clarified changes in the contents of polar metabolites (amino acids, organic acids, saccharides, cyclitols, and phosphoric acid) in leaf senescence in Ginkgo biloba with or without the application of methyl jasmonate (JA-Me) in comparison with those in naturally senescent leaf blades and petioles. The contents of most amino acids and citric and malic acids were significantly higher in abaxially, and that of myo-inositol was lower in abaxially JA-Me-treated leaves than in adaxially JA-Me-treated and naturally senescent leaves. The levels of succinic and fumaric acids in leaves treated adaxially substantially high, but not in naturally senescent leaves. In contrast, sucrose, glucose, and fructose contents were much lower in leaf blades and petioles treated abaxially with JA-Me than those treated adaxially. The levels of these saccharides were also lower compared with those in naturally senescent leaves. Shikimic acid and quinic acid were present at high levels in leaf blades and petioles of G. biloba. In leaves naturally senescent, their levels were higher compared to green leaves. The shikimic acid content was also higher in the organs of naturally yellow leaves than in those treated with JA-Me. These results strongly suggest that JA-Me applied abaxially significantly enhanced processes of primary metabolism during senescence of G. biloba compared with those applied adaxially. The changes in polar metabolites in relation to natural senescence were also discussed. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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13 pages, 2130 KiB

Open AccessArticle

Identification of Phytaspase Interactors via the Proximity-Dependent Biotin-Based Identification Approach

by Anastasia D. Teplova, Marina V. Serebryakova, Raisa A. Galiullina, Nina V. Chichkova and Andrey B. Vartapetian

Int. J. Mol. Sci. 2021, 22(23), 13123; https://doi.org/10.3390/ijms222313123 - 04 Dec 2021

Cited by 5 | Viewed by 1992

Abstract

Proteolytic enzymes are instrumental in various aspects of plant development, including senescence. This may be due not only to their digestive activity, which enables protein utilization, but also to fulfilling regulatory functions. Indeed, for the largest family of plant serine proteases, subtilisin-like proteases (subtilases), several members of which have been implicated in leaf and plant senescence, both non-specific proteolysis and regulatory protein processing have been documented. Here, we strived to identify the protein partners of phytaspase, a plant subtilase involved in stress-induced programmed cell death that possesses a characteristic aspartate-specific hydrolytic activity and unusual localization dynamics. A proximity-dependent biotin identification approach in Nicotiana benthamiana leaves producing phytaspase fused to a non-specific biotin ligase TurboID was employed. Although the TurboID moiety appeared to be unstable in the apoplast environment, several intracellular candidate protein interactors of phytaspase were identified. These were mainly, though not exclusively, represented by soluble residents of the endoplasmic reticulum, namely endoplasmin, BiP, and calreticulin-3. For calreticultin-3, whose gene is characterized by an enhanced expression in senescing leaves, direct interaction with phytaspase was confirmed in an in vitro binding assay using purified proteins. In addition, an apparent alteration of post-translational modification of calreticultin-3 in phytaspase-overproducing plant cells was observed. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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14 pages, 2912 KiB

Open AccessArticle

Altered Expression of OsAAP3 Influences Rice Lesion Mimic and Leaf Senescence by Regulating Arginine Transport and Nitric Oxide Pathway

by Qilang Wei, Zhenwei Yan, Yifan Xiong and Zhongming Fang

Int. J. Mol. Sci. 2021, 22(4), 2181; https://doi.org/10.3390/ijms22042181 - 22 Feb 2021

Cited by 14 | Viewed by 2455

Abstract

Persistent lesion mimic can cause leaf senescence, affecting grain yield in crops. However, knowledge about the regulation of lesion mimic and leaf senescence in crop plants is still limited. Here, we report that the amino acid transporter OsAAP3, a negative regulator of tiller bud elongation and rice grain yield, is involved in lesion mimic and leaf senescence. Altered expression of OsAAP3 can initiate the nitric oxide signaling pathway through excessive accumulation of arginine in rice leaves, influencing ROS accumulation, antioxidant enzymes activities, proline concentration, and malondialdehyde concentration. This finally triggers cell death which ultimately leads to lesion mimic and leaf senescence by regulating the degradation of chloroplast and the expression abundance of components in the photosynthetic pathway. Overall, the results not only provide initial insights into the regulatory role of amino acid transport genes in rice growth and development, but also help to understand the factors regulating the leaf senescence. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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13 pages, 2426 KiB

Open AccessArticle

Arabidopsis Phototropins Participate in the Regulation of Dark-Induced Leaf Senescence

by Aleksandra Eckstein, Joanna Grzyb, Paweł Hermanowicz, Piotr Zgłobicki, Justyna Łabuz, Wojciech Strzałka, Dariusz Dziga and Agnieszka Katarzyna Banaś

Int. J. Mol. Sci. 2021, 22(4), 1836; https://doi.org/10.3390/ijms22041836 - 12 Feb 2021

Cited by 4 | Viewed by 2464

Abstract

Senescence is the final stage of plant development, affecting individual organs or the whole organism, and it can be induced by several environmental factors, including shading or darkness. Although inevitable, senescence is a complex and tightly regulated process, ensuring optimal remobilization of nutrients and cellular components from senescing organs. Photoreceptors such as phytochromes and cryptochromes are known to participate in the process of senescence, but the involvement of phototropins has not been studied to date. We investigated the role of these blue light photoreceptors in the senescence of individually darkened Arabidopsis thaliana leaves. We compared several physiological and molecular senescence markers in darkened leaves of wild-type plants and phototropin mutants (phot1, phot2, and phot1phot2). In general, all the symptoms of senescence (lower photochemical activity of photosystem II, photosynthetic pigment degradation, down-regulation of photosynthetic genes, and up-regulation of senescence-associated genes) were less pronounced in phot1phot2, as compared to the wild type, and some also in one of the single mutants, indicating delayed senescence. This points to different mechanisms of phototropin operation in the regulation of senescence-associated processes, either with both photoreceptors acting redundantly, or only one of them, phot1, playing a dominant role. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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10 pages, 2176 KiB

Open AccessArticle

SATMF Suppresses the Premature Senescence Phenotype of the ATM Loss-of-Function Mutant and Improves Its Fertility in Arabidopsis

by Yi Zhang, Hou-Ling Wang, Yuhan Gao, Hongwei Guo and Zhonghai Li

Int. J. Mol. Sci. 2020, 21(21), 8120; https://doi.org/10.3390/ijms21218120 - 30 Oct 2020

Cited by 4 | Viewed by 2305

Abstract

Leaf senescence is the final stage of leaf development. It is accompanied by the remobilization of nutrients from senescent leaves to developing organs. The occurrence of senescence is the consequence of integrating intrinsic and environmental signals. DNA damage triggered by stresses has been regarded as one of the reasons for senescence. To prevent DNA damage, cells have evolved elaborate DNA repair machinery. The ataxia telangiectasia mutated (ATM) functions as the chief transducer of the double-strand breaks (DSBs) signal. Our previous study suggests that ATM functions in lifespan regulation in Arabidopsis. However, ATM regulatory mechanism on plant longevity remains unclear. Here, we performed chemical mutagenesis to identify the components involved in ATM-mediated longevity and obtained three dominant mutants satmf1~3, suppressor of atm in fertility, displaying delayed senescence and restored fertility in comparison with atm mutant. Molecular cloning and functional analysis of SATMF (suppressor of atm in fertility) will help to understand the underlying regulatory mechanism of ATM in plants, and shed light on developing new treatments for the disease Ataxia-telangiectasia. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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18 pages, 5019 KiB

Open AccessArticle

Wheat Transcription Factor TaSNAC11-4B Positively Regulates Leaf Senescence through Promoting ROS Production in Transgenic Arabidopsis

by Zenglin Zhang, Chen Liu and Yongfeng Guo

Int. J. Mol. Sci. 2020, 21(20), 7672; https://doi.org/10.3390/ijms21207672 - 16 Oct 2020

Cited by 14 | Viewed by 2683

Abstract

Senescence is the final stage of leaf development which is accompanied by highly coordinated and complicated reprogramming of gene expression. Genetic manipulation of leaf senescence in major crops including wheat has been shown to be able to increase stress tolerance and grain yield. NAC(No apical meristem (NAM), ATAF1/2, and cup-shaped cotyledon (CUC)) transcription factors (TFs) play important roles in regulating gene expression changes during leaf senescence and in response to abiotic stresses. Here, we report the characterization of TaSNAC11-4B (Uniprot: A0A1D5XI64), a wheat NAC family member that acts as a functional homolog of AtNAP, a key regulator of leaf senescence in Arabidopsis. The expression of TaSNAC11-4B was up-regulated with the progression of leaf senescence, in response to abscisic acid (ABA) and drought treatments in wheat. Ectopic expression of TaSNAC11-4B in Arabidopsis promoted ROS accumulation and significantly accelerated age-dependent as well as drought- and ABA-induced leaf senescence. Results from transcriptional activity assays indicated that the TaSNAC11-4B protein displayed transcriptional activation activities that are dependent on its C terminus. Furthermore, qRT-PCR and dual-Luciferase assay results suggested that TaSNAC11-4B could positively regulate the expression of AtrbohD and AtrbohF, which encode catalytic subunits of the ROS-producing NADPH oxidase. Further analysis of TaSNAC11-4B in wheat senescence and the potential application of this gene in manipulating leaf senescence with the purpose of yield increase and stress tolerance is discussed. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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Review

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22 pages, 947 KiB

Open AccessReview

Senescence-Associated Glycine max (Gm)NAC Genes: Integration of Natural and Stress-Induced Leaf Senescence

by Otto Teixeira Fraga, Bruno Paes de Melo, Iana Pedro Silva Quadros, Pedro Augusto Braga Reis and Elizabeth Pacheco Batista Fontes

Int. J. Mol. Sci. 2021, 22(15), 8287; https://doi.org/10.3390/ijms22158287 - 01 Aug 2021

Cited by 18 | Viewed by 3977

Abstract

Leaf senescence is a genetically regulated developmental process that can be triggered by a variety of internal and external signals, including hormones and environmental stimuli. Among the senescence-associated genes controlling leaf senescence, the transcriptional factors (TFs) comprise a functional class that is highly active at the onset and during the progression of leaf senescence. The plant-specific NAC (NAM, ATAF, and CUC) TFs are essential for controlling leaf senescence. Several members of Arabidopsis AtNAC-SAGs are well characterized as players in elucidated regulatory networks. However, only a few soybean members of this class display well-known functions; knowledge about their regulatory circuits is still rudimentary. Here, we describe the expression profile of soybean GmNAC-SAGs upregulated by natural senescence and their functional correlation with putative AtNAC-SAGs orthologs. The mechanisms and the regulatory gene networks underlying GmNAC081- and GmNAC030-positive regulation in leaf senescence are discussed. Furthermore, new insights into the role of GmNAC065 as a negative senescence regulator are presented, demonstrating extraordinary functional conservation with the Arabidopsis counterpart. Finally, we describe a regulatory circuit which integrates a stress-induced cell death program with developmental leaf senescence via the NRP-NAC-VPE signaling module. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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19 pages, 1533 KiB

Open AccessReview

Current Understanding of Leaf Senescence in Rice

by Sichul Lee and Celine Masclaux-Daubresse

Int. J. Mol. Sci. 2021, 22(9), 4515; https://doi.org/10.3390/ijms22094515 - 26 Apr 2021

Cited by 43 | Viewed by 4804

Abstract

Leaf senescence, which is the last developmental phase of plant growth, is controlled by multiple genetic and environmental factors. Leaf yellowing is a visual indicator of senescence due to the loss of the green pigment chlorophyll. During senescence, the methodical disassembly of macromolecules occurs, facilitating nutrient recycling and translocation from the sink to the source organs, which is critical for plant fitness and productivity. Leaf senescence is a complex and tightly regulated process, with coordinated actions of multiple pathways, responding to a sophisticated integration of leaf age and various environmental signals. Many studies have been carried out to understand the leaf senescence-associated molecular mechanisms including the chlorophyll breakdown, phytohormonal and transcriptional regulation, interaction with environmental signals, and associated metabolic changes. The metabolic reprogramming and nutrient recycling occurring during leaf senescence highlight the fundamental role of this developmental stage for the nutrient economy at the whole plant level. The strong impact of the senescence-associated nutrient remobilization on cereal productivity and grain quality is of interest in many breeding programs. This review summarizes our current knowledge in rice on (i) the actors of chlorophyll degradation, (ii) the identification of stay-green genotypes, (iii) the identification of transcription factors involved in the regulation of leaf senescence, (iv) the roles of leaf-senescence-associated nitrogen enzymes on plant performance, and (v) stress-induced senescence. Compiling the different advances obtained on rice leaf senescence will provide a framework for future rice breeding strategies to improve grain yield. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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13 pages, 447 KiB

Open AccessReview

Low Light/Darkness as Stressors of Multifactor-Induced Senescence in Rice Plants

by Ahmed G. Gad, Habiba, Xiangzi Zheng and Ying Miao

Int. J. Mol. Sci. 2021, 22(8), 3936; https://doi.org/10.3390/ijms22083936 - 11 Apr 2021

Cited by 9 | Viewed by 2583

Abstract

Leaf senescence, as an integral part of the final development stage for plants, primarily remobilizes nutrients from the sources to the sinks in response to different stressors. The premature senescence of leaves is a critical challenge that causes significant economic losses in terms of crop yields. Although low light causes losses of up to 50% and affects rice yield and quality, its regulatory mechanisms remain poorly elucidated. Darkness-mediated premature leaf senescence is a well-studied stressor. It initiates the expression of senescence-associated genes (SAGs), which have been implicated in chlorophyll breakdown and degradation. The molecular and biochemical regulatory mechanisms of premature leaf senescence show significant levels of redundant biomass in complex pathways. Thus, clarifying the regulatory mechanisms of low-light/dark-induced senescence may be conducive to developing strategies for rice crop improvement. This review describes the recent molecular regulatory mechanisms associated with low-light response and dark-induced senescence (DIS), and their effects on plastid signaling and photosynthesis-mediated processes, chloroplast and protein degradation, as well as hormonal and transcriptional regulation in rice. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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16 pages, 1696 KiB

Open AccessReview

Light-Mediated Regulation of Leaf Senescence

by Yasuhito Sakuraba

Int. J. Mol. Sci. 2021, 22(7), 3291; https://doi.org/10.3390/ijms22073291 - 24 Mar 2021

Cited by 21 | Viewed by 4251

Abstract

Light is the primary regulator of various biological processes during the plant life cycle. Although plants utilize photosynthetically active radiation to generate chemical energy, they possess several photoreceptors that perceive light of specific wavelengths and then induce wavelength-specific responses. Light is also one of the key determinants of the initiation of leaf senescence, the last stage of leaf development. As the leaf photosynthetic activity decreases during the senescence phase, chloroplasts generate a variety of light-mediated retrograde signals to alter the expression of nuclear genes. On the other hand, phytochrome B (phyB)-mediated red-light signaling inhibits the initiation of leaf senescence by repressing the phytochrome interacting factor (PIF)-mediated transcriptional regulatory network involved in leaf senescence. In recent years, significant progress has been made in the field of leaf senescence to elucidate the role of light in the regulation of nuclear gene expression at the molecular level during the senescence phase. This review presents a summary of the current knowledge of the molecular mechanisms underlying light-mediated regulation of leaf senescence. Full article

(This article belongs to the Special Issue Molecular Mechanisms of Leaf Senescence)

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