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Members of the CEP (C-terminally Encoded Peptide) gene family have been shown to be involved in various developmental processes and stress responses in plants. In order to understand the roles of CEP peptides in stress response, a comprehensive bioinformatics approach was employed to identify NtCEP genes in tobacco (Nicotiana tabacum L.) and to analyze their potential roles in stress responses. Totally 21 NtCEP proteins were identified and categorized into two subgroups based on their CEP domains. Expression changes of the NtCEP genes in response to various abiotic stresses were analyzed via qRT-PCR and the results showed that a number of NtCEPs were significant up-regulated under drought, salinity, or temperature stress conditions. Furthermore, application of synthesized peptides derived from NtCEP5, NtCEP13, NtCEP14, and NtCEP17 enhanced plant tolerance to different salt stress treatments. NtCEP5, NtCEP9 and NtCEP14, and NtCEP17 peptides were able to promote osmotic tolerance of tobacco plants. The results from this study suggest that NtCEP peptides may serve as important signaling molecules in tobacco's response to abiotic stresses.

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Formins or formin homology 2 (FH2) proteins, evolutionarily conserved multi-domain proteins in eukaryotes, serve as pivotal actin organizers, orchestrating the structure and dynamics of the actin cytoskeleton. However, a comprehensive investigation into the formin family and their plausible involvement in abiotic stress remains undocumented in soybean (Glycine max). In the current study, 34 soybean FH (GmFH)family members were discerned, their genomic distribution spanning the twenty chromosomes in a non-uniform pattern. Evolutionary analysis of the FH gene family across plant species delineated five discernible groups (Group I to V) and displayed a closer evolutionary relationship within Glycine soja, Glycine max, and Arabidopsis thaliana. Analysis of the gene structure of GmFH unveiled variable sequence lengths and substantial diversity in conserved motifs. Structural prediction in the promoter regions of GmFH gene suggested a large set of cis-acting elements associated with hormone signaling, plant growth and development, and stress responses. The investigation of the syntenic relationship revealed a greater convergence of GmFH genes with dicots, indicating a close evolutionary affinity. Transcriptome data unveiled distinctive expression patterns of several GmFH genes across diverse plant tissues and developmental stages, underscoring a spatiotemporal regulatory framework governing the transcriptional dynamics of GmFH gene. Gene expression and qRT-PCR analysis identified many GmFH genes with a dynamic pattern in response to abiotic stresses, revealing their potential roles in regulating plant stress adaptation. Additionally, protein interaction analysis highlighted an intricate web of interactions among diverse GmFH proteins. These findings collectively underscore a novel biological function of GmFH proteins in facilitating stress adaptation in soybeans.

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As the final stage of leaf development, leaf senescence is affected by a variety of internal and external signals including age and environmental stresses. Although significant progress has been made in elucidating the mechanisms of age-dependent leaf senescence, it is not clear how stress conditions induce a similar process. Here, we report the roles of a stress-responsive and senescence-induced gene, ERD7 (EARLY RESPONSIVE TO DEHYDRATION 7), in regulating both age-dependent and stress-induced leaf senescence in Arabidopsis. The results showed that the leaves of erd7 mutant exhibited a significant delay in both age-dependent and stress-induced senescence, while transgenic plants overexpressing the gene exhibited an obvious accelerated leaf senescence. Furthermore, based on the results of LC-MS/MS and PRM quantitative analyses, we selected two phosphorylation sites, Thr-225 and Ser-262, which have a higher abundance during senescence, and demonstrated that they play a key role in the function of ERD7 in regulating senescence. Transgenic plants overexpressing the phospho-mimetic mutant of the activation segment residues ERD7T225D and ERD7T262D exhibited a significantly early senescence, while the inactivation segment ERD7T225A and ERD7T262A displayed a delayed senescence. Moreover, we found that ERD7 regulates ROS accumulation by enhancing the expression of AtrbohD and AtrbohF, which is dependent on the critical residues, i.e., Thr-225 and Ser-262. Our findings suggest that ERD7 is a positive regulator of senescence, which might function as a crosstalk hub between age-dependent and stress-induced leaf senescence.

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Receptor-like kinases (RLKs) are the most important class of cell surface receptors, and play crucial roles in plant development and stress responses. However, few studies have been reported about the biofunctions of RLKs in leaf senescence. Here, we characterized a novel Arabidopsis RLK-encoding gene, SENESCENCE-RELATED RECEPTOR KINASE 1 (SENRK1), which was significantly down-regulated during leaf senescence. Notably, the loss-of-function senrk1 mutants displayed an early leaf senescence phenotype, while overexpression of SENRK1 significantly delayed leaf senescence, indicating that SENRK1 negatively regulates age-dependent leaf senescence in Arabidopsis. Furthermore, the senescence-promoting transcription factor WRKY53 repressed the expression of SENRK1. While the wrky53 mutant showed a delayed senescence phenotype as previously reported, the wrky53 senrk1-1 double mutant exhibited precocious leaf senescence, suggesting that SENRK1 functions downstream of WRKY53 in regulating age-dependent leaf senescence in Arabidopsis.

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[This corrects the article DOI: 10.3389/fpls.2022.1000297.].

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Small secreted peptides (SSPs) are important signals for cell-to-cell communication in plant, involved in a variety of growth and developmental processes, as well as responses to stresses. While a large number of SSPs have been identified and characterized in various plant species, little is known about SSPs in wheat, one of the most important cereal crops. In this study, 4,981 putative SSPs were identified on the wheat genome, among which 1,790 TaSSPs were grouped into 38 known SSP families. The result also suggested that a large number of the putaitive wheat SSPs, Cys-rich peptides in particular, remained to be characterized. Several TaSSP genes were found to encode multiple SSP domains, including CLE, HEVEIN and HAIRPININ domains, and two potentially novel TaSSP family DYY and CRP8CI were identified manually among unpredicted TaSSPs. Analysis on the transcriptomic data showed that a great proportion of TaSSPs were expressed in response to abiotic stresses. Exogenous application of the TaCEPID peptide encoded by TraesCS1D02G130700 enhanced the tolerance of wheat plants to drought and salinity, suggesting porential roles of SSPs in regulating stress responses in wheat.

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NAC proteins constitute one of the largest transcription factor families and are involved in regulation of plant development and stress responses. Our previous transcriptome analyses of tobacco revealed a significant increase in the expression of NtNAC028 during leaf yellowing. In this study, we found that NtNAC028 was rapidly upregulated in response to high salinity, dehydration, and abscisic acid (ABA) stresses, suggesting a vital role of this gene in abiotic stress response. NtNAC028 loss-of-function tobacco plants generated via CRISPR-Cas9 showed delayed leaf senescence and increased tolerance to drought and salt stresses. Meanwhile NtNAC028 overexpression led to precocious leaf senescence and hypersensitivity to abiotic stresses in Arabidopsis, indicating that NtNAC028 functions as a positive regulator of natural leaf senescence and a negative regulator of stress tolerance. Furthermore, NtNAC028-overexpressing Arabidopsis plants showed lower antioxidant enzyme activities, higher reactive oxygen species (ROS), and H2O2 accumulation under high salinity, resulted in more severe oxidative damage after salt stress treatments. On the other hand, NtNAC028 mutation in tobacco resulted in upregulated expression of ROS-scavenging and abiotic stress-related genes, higher antioxidant enzyme activities, and enhanced tolerance against abiotic stresses, suggesting that NtNAC028 might act as a vital regulator for plant stress response likely by mediating ROS scavenging ability. Collectively, our results indicated that the NtNAC028 plays a key regulatory role in leaf senescence and response to multiple abiotic stresses.

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Leaf senescence is a highly coordinated process and has a significant impact on agriculture. Plant peptides are known to act as important cell-to-cell communication signals that are involved in multiple biological processes such as development and stress responses. However, very limited number of peptides has been reported to be associated with leaf senescence. Here, we report the characterization of the INFLORESCENCE DEFICIENT IN ABSCISSION-LIKE6 (IDL6) peptide as a regulator of leaf senescence. The expression of IDL6 was up-regulated in senescing leaves. Exogenous application of synthetic IDL6 peptides accelerated the process of leaf senescence. The idl6 mutant plants showed delayed natural leaf senescence as well as senescence included by darkness, indicating a regulatory role of IDL6 peptides in leaf senescence. The role of IDL6 as a positive regulator of leaf senescence was further supported by the results of overexpression analysis and complementation test. Transcriptome analysis revealed differential expression of phytohormone-responsive genes in idl6 mutant plants. Further analysis indicated that altered expression of IDL6 led to changes in leaf senescence phenotypes induced by ABA and ethylene treatments. The results from this study suggest that the IDL6 peptide positively regulates leaf senescence in Arabidopsis thaliana.

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Leaf senescence is an important developmental process in the plant life cycle and has a significant impact on agriculture. When facing harsh environmental conditions, monocarpic plants often initiate early leaf senescence as an adaptive mechanism to ensure a complete life cycle. Upon initiation, the senescence process is fine-tuned through the coordination of both positive and negative regulators. Here, we report that the small secreted peptide CLAVATA3/ESR-RELATED 14 (CLE14) functions in the suppression of leaf senescence by regulating ROS homeostasis in Arabidopsis. Expression of the CLE14-encoding gene in leaves was significantly induced by age, high salinity, abscisic acid (ABA), salicylic acid, and jasmonic acid. CLE14 knockout plants displayed accelerated progression of both natural and salinity-induced leaf senescence, whereas increased CLE14 expression or treatments with synthetic CLE14 peptides delayed senescence. CLE14 peptide treatments also delayed ABA-induced senescence in detached leaves. Further analysis showed that overexpression of CLE14 led to reduced ROS levels in leaves, where higher expression of ROS scavenging genes was detected. Moreover, CLE14 signaling resulted in transcriptional activation of JUB1, a NAC family transcription factor previously identified as a negative regulator of senescence. Notably, the delay of leaf senescence, reduction in H2O2 level, and activation of ROS scavenging genes by CLE14 peptides were dependent on JUB1. Collectively, these results suggest that the small peptide CLE14 serves as a novel "brake signal" to regulate age-dependent and stress-induced leaf senescence through JUB1-mediated ROS scavenging.

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The inflorescence deficient in abscission-like (IDL) genes have been shown to play critical roles in floral organ abscission, lateral root formation and various stress responses in Arabidopsis. The IDL gene family has been characterized in a number of plant species, while limited information is available about IDL genes of tobacco. In the current study, 15 NtIDL members were identified in the tobacco genome, and were classified into six groups together with IDL members from other species. Evolution analysis suggested that the NtIDL members form group VI might have originated from duplication events. Notably, NtIDL06 shared high similarities with AtIDA in the EPIP sequence, and its encoding gene was highly expressed in the abscission zone of flowers at late developmental stages, implying that NtIDL06 might regulate tobacco flower abscission. In addition, the results from cis-elements analysis of promoters and expression after stress treatments suggested that NtIDL members might be involved in various stress responses of tobacco. The results from this study provide information for further functional analysis related to flower abscission and stress responses of NtIDL genes.

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Proso millet (Panicum miliaceum L.) is a minor cereal crop that has been considered as health-promoting food. Little information is available however, about the metabolic basis of nutritional values of proso millet. In this study, using a UHPLC-QqQ-MS/MS-based metabolomics approach, we compared the metabolomes of whole grains from four proso millet varieties with different bran color, namely White, Black, Gray and Red. In total, 672 metabolites were identified, among which 121, 116 and 148 metabolites showed differential accumulation in the three comparison groups (White vs. Black/Gray/Red). The results demonstrated the main pathways that were differentially activated included: tryptophan metabolism, flavonoid, isoflavonoid, flavone, and flavonol biosynthesis. Considerable difference between varieties was observed in accumulation of phenolic acids and flavonoids, which might lead to difference in antioxidant activities. The results of this study provide useful information for further investigation of proso millet food chemistry and for sufficient utilization of this special crop.

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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.

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Leaf senescence is a programmed developmental process regulated by various endogenous and exogenous factors. Here we report the characterization of the senescence-regulating role of DEAR4 (AT4G36900) from the DREB1/CBF (dehydration-responsive element binding protein 1/C-repeat binding factor) family in Arabidopsis. The expression of DEAR4 is associated with leaf senescence and can be induced by ABA, JA, darkness, drought and salt stress. Transgenic plants over-expressing DEAR4 showed a dramatically enhanced leaf senescence phenotype under normal and dark conditions while the dear4 knock-down mutant displayed delayed senescence. DEAR4 over-expressing plants showed decreased seed germination rate under ABA and salt stress conditions as well as decreased drought tolerance, indicating that DEAR4 was involved in both senescence and stress response processes. Furthermore, we found that DEAR4 protein displayed transcriptional repressor activities in yeast cells. DEAR4 could directly repress the expression of a subset of COLD-REGULATED (COR) and RESPONSIVE TO DEHYDRATION (RD) genes which have been shown to be involved in leaf longevity and stress response. Also we found that DERA4 could induce the production of Reactive oxygen species (ROS), the common signal of senescence and stress responses, which gives us the clue that DEAR4 may play an integrative role in senescence and stress response via regulating ROS production.

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Leaf senescence is regulated by a large number of internal and environmental factors. Here, we report that AtUSR1 (U-box Senescence Related 1) which encodes a plant Ring/U-box protein, is involved in age-dependent and dark-induced leaf senescence in Arabidopsis. Expression of AtUSR1 gene in leaves was up-regulated in darkness and during aging. Plants of usr1, an AtUSR1 gene knock-down mutant, showed a significant delay in age-dependent and dark-induced leaf senescence and the delayed senescence phenotype was rescued when the AtUSR1 gene was transferred back to the mutant plants. Meanwhile, overexpression of AtUSR1 caused accelerated leaf senescence. Furthermore, the role of AtUSR1 in regulating leaf senescence is related to MYC2-mediuated jasmonic acid (JA) signaling pathway. MeJA treatments promoted the accumulation of AtUSR1 transcripts and this expression activation was dependent on the function of MYC2, a key transcription factor in JA signaling. Dual-luciferase assay results indicated that MYC2 promoted the expression of AtUSR1. Overexpression of AtUSR1 in myc2 mutant plants showed precocious senescence, while myc2 mutation alone caused a delay in leaf senescence, suggesting that AtUSR1 functions downstream to MYC2 in the JA signaling pathway in promoting leaf senescence.

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As the last stage of plant development, leaf senescence has a great impact on plant's life cycle. Genetic manipulation of leaf senescence has been used as an efficient approach in improving the yield and quality of crop plants. Here we describe an ethyl methane sulfonate (EMS) mutagenesis induced premature leaf senescence mutant yellow leaf 1 (yl1) in common tobacco (Nicotiana tabacum L.). The yl1 plants displayed early leaf yellowing. Physiological parameters and marker genes expression indicated that the yl1 phenotype was caused by premature leaf senescence. Genetic analyses indicated that the yl1 phenotype was controlled by a single recessive gene that was subsequently mapped to a specific interval of tobacco linkage group 11 using simple sequence repeat (SSR) markers. Exogenous plant hormone treatments of leaves showed that the yl1 mutant was more sensitive to ethylene and jasmonic acid than the wild type. No similar tobacco premature leaf senescence mutants have been reported. This study laid a foundation for finding the gene controlling the mutation phenotype and revealing the molecular regulation mechanism of tobacco leaf senescence in the next stage.

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As the last stage of plant development, senescence can be regulated by a large number of signals such as aging, reproductive growth, nutrient availability, and stresses. Various plant hormones have been shown to be involved in regulating plant senescence. For example, ethylene, abscisic acid (ABA), jasmonic acid (JA), salicylic acid (SA), and strigolactones (SLs) promote senescence, whereas cytokinins (CKs) inhibit senescence. Different hormones regulate senescence via distinct pathways, while cross talks between signaling pathways exist. In senescence-related studies, treating plants with various hormones to alter senescence is a common practice. In this chapter, we summarize experimental procedures of treating detached Arabidopsis leaves with a number of senescence-regulating hormones including ABA, SLs, MeJA, SA peptide hormones.

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The NAC family is one of the largest families of plant-specific transcription factors (TFs) and NAC proteins play important regulatory roles in a variety of developmental and stress response processes in plants. Members of the NAC family TFs have been shown to be important regulators of leaf senescence in a number of plant species. Here we report the identification of the NAC family in tobacco (Nicotiana tabacum) and characterization of the potential role of some of the tobacco NAC TFs in regulating leaf senescence. A total of 154 NAC genes (NtNACs) were identified and clustered together with the Arabidopsis NAC family into fifteen groups (a-o). Transcriptome data analysis followed by qRT-PCR validation showed that the majority of the senescence-up-regulated NtNACs fall into subgroups NAC-b and f. A number of known senescence regulators from Arabidopsis also belong to these two subgroups. Among these senescence-up-regulated NtNACs, NtNAC080, a close homolog of AtNAP, is a positive regulator of leaf senescence. Overexpression of NtNAC080 caused early senescence in Arabidopsis leaves and NtNAC080 mutation induced by Cas9/gRNA in tobacco led to delayed leaf senescence.

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Leaf senescence in plants is a coordinated process that involves remobilization of nutrients from senescing leaves to sink tissues. The molecular events associated with nutrient remobilization are however not well understood. In this study the tobacco system with a source-sink relationship between different leaf positions was used in analyzing the spatiotemporal changes of 76 metabolites from leaves at 3 different stalk positions and 8 developmental stages. The metabolomic data was then compared with RNA-seq data from the same samples to analyze the activities of the metabolic pathways that are important for nutrient remobilization. Integrative analyses on metabolites accumulation and expression changes of enzyme-encoding genes in corresponding metabolic pathways indicated a significant up-regulation of the tricarboxylic acid cycle and related metabolism of sugars, amino acids and fatty acids, suggesting the importance of energy metabolism during leaf senescence. Other changes of the metabolism during tobacco leaf senescence include increased activities of the GS/GOGAT cycle which is responsible for nitrogen recycling, and increased accumulation of nicotine. The results also suggested that a number of compounds seemed to be transported from senescing leaves at lower positions to sink leaves at upper positions. Some of these metabolites could play a role in nutrient remobilization.

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Members of the plant-specific WOX transcription factor family have been reported to play important roles in cell to cell communication as well as other physiological and developmental processes. In this study, ten members of the WOX transcription factor family were identified in Solanum lycopersicum with HMMER. Neighbor-joining phylogenetic tree, maximum-likelihood tree and Bayesian-inference tree were constructed and similar topologies were shown using the protein sequences of the homeodomain. Phylogenetic study revealed that the 25 WOX family members from Arabidopsis and tomato fall into three clades and nine subfamilies. The patterns of exon-intron structures and organization of conserved domains in Arabidopsis and tomato were consistent based on the phylogenetic results. Transcriptome analysis showed that the expression patterns of SlWOXs were different in different tissue types. Gene Ontology (GO) analysis suggested that, as transcription factors, the SlWOX family members could be involved in a number of biological processes including cell to cell communication and tissue development. Our results are useful for future studies on WOX family members in tomato and other plant species.

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