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Abscisic Acid and Jasmonate Metabolisms Are Jointly Regulated During Senescence in Roots and Leaves of Populus trichocarpa.

ABSTRACT: Plant senescence is a highly regulated process that allows nutrients to be mobilized from dying tissues to other organs. Despite that senescence has been extensively studied in leaves, the senescence of ephemeral organs located underground is still poorly understood, especially in the context of phytohormone engagement. The present study focused on filling this knowledge gap by examining the roles of abscisic acid (ABA) and jasmonate in the regulation of senescence of fine, absorptive roots and leaves of Populus trichocarpa. Immunohistochemical (IHC), chromatographic, and molecular methods were utilized to achieve this objective. A transcriptomic analysis identified significant changes in gene expression that were associated with the metabolism and signal transduction of phytohormones, especially ABA and jasmonate. The increased level of these phytohormones during senescence was detected in both organs and was confirmed by IHC. Based on the obtained data, we suggest that phytohormonal regulation of senescence in roots and leaves is organ-specific. We have shown that the regulation of ABA and JA metabolism is tightly regulated during senescence processes in both leaves and roots. The results were discussed with respect to the role of ABA in cold tolerance and the role of JA in resistance to pathogens.

SUBMITTER: Wojciechowska N

PROVIDER: S-EPMC7139941 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Abscisic Acid and Jasmonate Metabolisms Are Jointly Regulated During Senescence in Roots and Leaves of <i>Populus trichocarpa</i>.

Wojciechowska Natalia N Wilmowicz Emilia E Marzec-Schmidt Katarzyna K Ludwików Agnieszka A Bagniewska-Zadworna Agnieszka A

International journal of molecular sciences 20200317 6

Plant senescence is a highly regulated process that allows nutrients to be mobilized from dying tissues to other organs. Despite that senescence has been extensively studied in leaves, the senescence of ephemeral organs located underground is still poorly understood, especially in the context of phytohormone engagement. The present study focused on filling this knowledge gap by examining the roles of abscisic acid (ABA) and jasmonate in the regulation of senescence of fine, absorptive roots and ...[more]

PMID: 32192046

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Project description:BackgroundSenescence, despite its destructive character, is a process that is precisely-regulated. The control of senescence is required to achieve remobilization of resources, a principle aspect of senescence. Remobilization allows plants to recapture valuable resources that would otherwise be lost to the environment with the senescing organ. Autophagy is one of the critical processes that is switched on during senescence. This evolutionarily conserved process plays dual, antagonistic roles. On the one hand, it counteracts instantaneous cell death and allows the process of remobilization to be set in motion, while on the other hand, it participates in the degradation of cellular components. Autophagy has been demonstrated to occur in many plant species during the senescence of leaves and flower petals. Little is known, however, about the senescence process in other ephemeral organs, such as fine roots, whose lifespan is also relatively short. We hypothesized that, like the case of seasonal leaf senescence, autophagy also plays a role in the senescence of fine roots, and that both processes are synchronized in their timing.ResultsWe evaluated which morphological and cytological symptoms are universal or unique in the senescence of fine roots and leaves. The results of our study confirmed that autophagy plays a key role in the senescence of fine roots, and is associated also with the process of cellular components degradation. In both organs, structures related to autophagy were observed, such as autophagic bodies and autophagosomes. The role of autophagy in the senescence of these plant organs was further confirmed by an analysis of ATG gene expression and protein detection.ConclusionsThe present study is the first one to examine molecular mechanisms associated with the senescence of fine roots, and provide evidence that can be used to determine whether senescence of fine roots can be treated as another example of developmentally programmed cell death (dPCD). Our results indicate that there is a strong similarity between the senescence of fine roots and other ephemeral organs, suggesting that this process occurs by the same autophagy-related mechanisms in all plant ephemeral organs.

Project description:We studied the changes that occur in gene transcription during seasonal senescence in Populus trichocarpa pioneer leaves and fine roots. Plant senescence is a strictly regulated physiological process that allows relocating of valuable nutrients from senescent tissues before death. It might be induced by internal or external factors and among them, phytohormones play an undoubtedly significant role. Senescence was extensively studied in leaves, but the aging of other ephemeral organs, located underground, and its drivers are still poorly understood. We focused on collective results to fill in the knowledge gap about senescence of fine, absorptive roots and leaves in order to check if there are universal mechanisms involved during plant organ senescence. Transcriptional profiling was conducted with the use of microarrays to identify genes involved in developmental PCD. Samples were collected three times during a growth season. The first collection was considered as a control and was collected in early summer (July 7–15) when leaves and the root system were fully developed and functional. The second group of leaf and root samples were harvested in early autumn (October 1–7) when chlorophyll levels in leaves had decreased by approximately 40% and when fine roots had changed in color from white to brown. The third group of samples were harvested in the middle of autumn (November 2–9) when chlorophyll levels in leaves decreased by approximately 65% and fine roots were dark brown or black color. Our results reveal the important role of phytohormones in regulating the senescence of both studied organs. The transcriptomic analyses showed significant changes in gene expression that are associated with phytohormones, especially with ABA and jasmonates. We conclude that phytohormonal regulation of senescence in roots and leaves is organ-specific. In roots, phytohormones are involved indirectly in regulation of senescence by increasing tolerance for cold or resistance for pathogens, whereas such correlation was not observed in leaves.

Project description:Histone deacetylases (HDACs) are key enzymes catalyzing the removal of acetyl groups from histones. HDACs act in concert with histone acetyltransferases (HATs) to regulate histone acetylation status, which modifies chromatin structure, affecting gene transcription and thus regulating multiple biological processes such as plant growth and development. Over a decade, certain HDACs in herbaceous plants have been deeply studied. However, functions of HDACs in woody plants are not well understood.Histone deacetylase specific inhibitor trichostatin A (TSA) was used to investigate the role of HDACs in organogenesis of roots and root development in Populus trochocarpa. The adventitious roots were regenerated and grown on medium supplemented with 0, 1, and 2.5 ?M TSA. TSA treatment delayed root regeneration and inhibited primary root growth. To examine the genes modified by TSA in the regenerated roots, tag-based digital gene expression (DGE) analysis was performed using Illumina HiSeqTM 2000. Approximately 4.5 million total clean tags were mapped per library. The distinct clean tags for the three libraries corresponding to 0, 1 and 2.5 ?M TSA treatment were 166167, 143103 and 153507, from which 38.45%, 31.84% and 38.88% were mapped unambiguously to the unigene database, respectively. Most of the tags were expressed at similar levels, showing a < 5-fold difference after 1 ?M and 2.5 ?M TSA treatments and the maximum fold-change of the tag copy number was around 20. The expression levels of many genes in roots were significantly altered by TSA. A total of 36 genes were up-regulated and 1368 genes were down-regulated after 1 ?M TSA treatment, while 166 genes were up-regulated and 397 genes were down-regulated after 2.5 ?M TSA treatment. Gene ontology (GO) and pathway analyses indicated that the differentially expressed genes were related to many kinds of molecular functions and biological processes. The genes encoding key enzymes catalyzing gibberellin biosynthesis were significantly down-regulated in the roots exposed to 2.5 ?M TSA and their expression changes were validated by using real-time PCR.HDACs were required for de novo organogenesis and normal growth of populus roots. DGE data provides the gene profiles in roots probably regulated by histone acetylation during root growth and development, which will lead to a better understanding of the mechanism controlling root development.

Project description:BACKGROUND:Limited data are available on the responses of reactive oxygen species (ROS) and methylglyoxal (MG) metabolisms to low pH in roots and leaves. In China, quite a few of Citrus are cultivated in acidic soils (pH < 5.0). 'Xuegan' (Citrus sinensis) and 'Sour pummelo' (Citrus grandis) (C. sinensis were more tolerant to low pH than C. grandis) seedlings were irrigated daily with nutrient solution at a pH of 2.5, 3 or 5 for nine months. Thereafter, we examined low pH effects on growth, and superoxide anion production rate (SAP), malondialdehyde (MDA), MG, antioxidants, and enzymes related to ROS and MG detoxification in roots and leaves in order to (a) test the hypothesis that low pH affected ROS and MG metabolisms more in roots than those of leaves, and (b) understand the roles of ROS and MG metabolisms in Citrus low pH-tolerance and -toxicity. RESULTS:Compared with control, most of the physiological parameters related to ROS and MG metabolisms were greatly altered at pH 2.5, but almost unaffected at pH 3. In addition to decreased root growth, many fibrous roots became rotten and died at pH 2.5. pH 2.5-induced changes in SAP, the levels of MDA, MG and antioxidants, and the activities of most enzymes related to ROS and MG metabolisms were greater in roots than those of leaves. Impairment of root ascorbate metabolism was the most serious, especially in C. grandis roots. pH 2.5-induced increases in MDA and MG levels in roots and leaves, decreases in the ratios of ascorbate/(ascorbate+dehydroascorbate) in roots and leaves and of reduced glutathione/(reduced+oxidized glutathione) in roots were greater in C. grandis than those in C. sinensis. CONCLUSIONS:Low pH affected MG and ROS metabolisms more in roots than those in leaves. The most seriously impaired ascorbate metabolism in roots was suggested to play a role in low pH-induced root death and growth inhibition. Low pH-treated C. sinensis roots and leaves had higher capacity to maintain a balance between ROS and MG production and their removal via detoxification systems than low pH-treated C. grandis ones, thus contribute to the higher acid-tolerance of C. sinensis.

Project description:BACKGROUND: SPLs, a family of transcription factors specific to plants, play vital roles in plant growth and development through regulation of various physiological and biochemical processes. Although Populus trichocarpa is a model forest tree, the PtSPL gene family has not been systematically studied. RESULTS: Here we report the identification of 28 full-length PtSPLs, which distribute on 14 P. trichocarpa chromosomes. Based on the phylogenetic relationships of SPLs in P. trichocarpa and Arabidopsis, plant SPLs can be classified into 6 groups. Each group contains at least a PtSPL and an AtSPL. The N-terminal zinc finger 1 (Zn1) of SBP domain in group 6 SPLs has four cysteine residues (CCCC-type), while Zn1 of SPLs in the other groups mainly contains three cysteine and one histidine residues (C2HC-type). Comparative analyses of gene structures, conserved motifs and expression patterns of PtSPLs and AtSPLs revealed the conservation of plant SPLs within a group, whereas among groups, the P. trichocarpa and Arabidopsis SPLs were significantly different. Various conserved motifs were identified in PtSPLs but not found in AtSPLs, suggesting the diversity of plant SPLs. A total of 11 pairs of intrachromosome-duplicated PtSPLs were identified, suggesting the importance of gene duplication in SPL gene expansion in P. trichocarpa. In addition, 18 of the 28 PtSPLs, belonging to G1, G2 and G5, were found to be targets of miR156. Consistently, all of the AtSPLs in these groups are regulated by miR156. It suggests the conservation of miR156-mediated posttranscriptional regulation in plants. CONCLUSIONS: A total of 28 full-length SPLs were identified from the whole genome sequence of P. trichocarpa. Through comprehensive analyses of gene structures, phylogenetic relationships, chromosomal locations, conserved motifs, expression patterns and miR156-mediated posttranscriptional regulation, the PtSPL gene family was characterized. Our results provide useful information for evolution and biological function of plant SPLs.

Dataset Information

Abscisic Acid and Jasmonate Metabolisms Are Jointly Regulated During Senescence in Roots and Leaves of Populus trichocarpa.

Publications

Abscisic Acid and Jasmonate Metabolisms Are Jointly Regulated During Senescence in Roots and Leaves of <i>Populus trichocarpa</i>.

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