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Ethylene-induced transcriptional and hormonal responses at the onset of sugarcane ripening.

ABSTRACT: The effects of ethephon as a sugarcane ripener are attributed to ethylene. However, the role of this phytohormone at the molecular level is unknown. We performed a transcriptome analysis combined with the evaluation of sucrose metabolism and hormone profiling of sugarcane plants sprayed with ethephon or aminoethoxyvinylglycine (AVG), an ethylene inhibitor, at the onset of ripening. The differential response between ethephon and AVG on sucrose level and sucrose synthase activity in internodes indicates ethylene as a potential regulator of sink strength. The correlation between hormone levels and transcriptional changes suggests ethylene as a trigger of multiple hormone signal cascades, with approximately 18% of differentially expressed genes involved in hormone biosynthesis, metabolism, signalling, and response. A defence response elicited in leaves favoured salicylic acid over the ethylene/jasmonic acid pathway, while the upper internode was prone to respond to ethylene with strong stimuli on ethylene biosynthesis and signalling genes. Besides, ethylene acted synergistically with abscisic acid, another ripening factor, and antagonistically with gibberellin and auxin. We identified potential ethylene target genes and characterized the hormonal status during ripening, providing insights into the action of ethylene at the site of sucrose accumulation. A molecular model of ethylene interplay with other hormones is proposed.

SUBMITTER: Cunha CP

PROVIDER: S-EPMC5339719 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Ethylene-induced transcriptional and hormonal responses at the onset of sugarcane ripening.

Cunha Camila P CP Roberto Guilherme G GG Vicentini Renato R Lembke Carolina G CG Souza Glaucia M GM Ribeiro Rafael V RV Machado Eduardo C EC Lagôa Ana M M A AM Menossi Marcelo M

Scientific reports 20170307

The effects of ethephon as a sugarcane ripener are attributed to ethylene. However, the role of this phytohormone at the molecular level is unknown. We performed a transcriptome analysis combined with the evaluation of sucrose metabolism and hormone profiling of sugarcane plants sprayed with ethephon or aminoethoxyvinylglycine (AVG), an ethylene inhibitor, at the onset of ripening. The differential response between ethephon and AVG on sucrose level and sucrose synthase activity in internodes ind ...[more]

PMID: 28266527

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Project description:BACKGROUND:Sugarcane is a major crop producing about 80% of sugar globally. Increasing sugar content is a top priority for sugarcane breeding programs worldwide, however, the progress is extremely slow. Owing to its commercial significance, the physiology of sucrose accumulation has been studied extensively but it did not lead to any significant practical outcomes. Recent molecular studies are beginning to recognize genes and gene networks associated with this phenomenon. To further advance our molecular understanding of sucrose accumulation, we altered sucrose content of sugarcane genotypes with inherently large variation for sucrose accumulation using a sugarcane ripener, ethylene, and studied their transcriptomes to identify genes associated with the phenomenon. RESULTS:Sucrose content variation in the experimental genotypes was substantial, with the top-performing clone producing almost 60% more sucrose than the poorest performer. Ethylene treatment increased stem sucrose content but that occurred only in low-sugar genotype. Transcriptomic analyses have identified about 160,000 unigenes of which 86,000 annotated genes were classified into functional groups associated with carbohydrate metabolism, signaling, localization, transport, hydrolysis, growth, catalytic activity, membrane and storage, suggesting the structural and functional specification, including sucrose accumulation, occurring in maturing internodes. About 25,000 genes were differentially expressed between all genotypes and treatments combined. Genotype had a dominant effect on differential gene expression than ethylene treatment. Sucrose and starch metabolism genes were more responsive to ethylene treatment in low-sugar genotype. Ethylene caused differential gene expression of many stress-related transcription factors, carbohydrate metabolism, hormone metabolism and epigenetic modification. Ethylene-induced expression of ethylene-responsive transcription factors, cytosolic acid- and cell wall-bound invertases, and ATPase was more pronounced in low- than in high-sugar genotype, suggesting an ethylene-stimulated sink activity and consequent increased sucrose accumulation in low-sugar genotype. CONCLUSION:Ethylene-induced sucrose accumulation is more pronounced in low-sugar sugarcane genotype, and this is possibly achieved by the preferential activation of genes such as invertases that increase sink strength in the stem. The relatively high enrichment of differentially expressed genes associated with hormone metabolism and signaling and stress suggests a strong hormonal regulation of source-sink activity, growth and sucrose accumulation in sugarcane.

Project description:BACKGROUND:The ripening of grape berry is generally regulated by abscisic acid (ABA), and has no relationship with ethylene function. However, functional interaction and synergism between ABA and ethylene during the beginning of grape berry ripening (véraison) has been found recently. RESULTS:The expressions of VvNCED1 encoding 9-cis-epoxycarotenoid dioxygenase (NCED) and VvGT encoding ABA glucosyltransferase were all increased rapidly at the stage of véraison and reached the highest level at 9th week after full bloom. However, VvCYP1 encoding ABA 8'-hydroxylase and Vv?G1 encoding berry ?-glucosidase are different, whose expression peak appeared at the 10th week after full bloom and in especial Vv?G1 remained at a high level till harvest. The VvACO1 encoding 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase, the VvETR2 (ethylene response 2) and VvCTR1 (constitutive triple response 1) had a transient expression peak at pre-véraison, while the VvEIN4 (ethylene insensitive 4) expression gradually increased from the véraison to one week before harvest stage. The above mentioned changes happened again in the berry after harvest. At one week before véraison, double block treatment with NiCl2 plus 1-methylcyclopropene (1-MCP) not only inhibited the release of ethylene and the expression of related genes but also suppressed the transcription of VvNCED1 and the synthesis of ABA which all might result in inhibiting the fruit ripening onset. Treatment with ABA could relieve the double block and restore fruit ripening course. However, after harvest, double block treatment with NiCl2 plus 1-MCP could not suppress the transcription of VvNCED1 and the accumulation of ABA, and also could not inhibit the start of fruit senescence. CONCLUSION:The trace endogenous ethylene induces the transcription of VvNCED1 and then the generation of ABA followed. Both ethylene and ABA are likely to be important and their interplaying may be required to start the process of berry ripening. When the level of ABA reached the peak value, part of it will be stored in the form of ABA-GE. While after harvest, abiotic stresses principally (such as dehydration, harvest shock) could induce the transcription of VvNCED1 and the accumulation of ABA, thus starting the process of fruit senescence.

Project description:In somatic embryogenesis, embryos are formed from a single or small group of somatic cells in response to stress and hormonal stimuli. In this study, a high-throughput phosphoproteomic analysis was used to identify and quantify phosphoproteins related to the acquisition of embryogenic competence in sugarcane. Embryogenic (EC) and nonembryogenic (NEC) calli were compared at the multiplication phase, resulting in the identification of 1279 phosphoproteins. After the differential accumulation analysis, 163 phosphoproteins were identified as unique to EC, and nine were unique to NEC, while 51 were upaccumulated, and 40 were downaccumulated in EC compared to NEC. These phosphopeptides were mainly single phosphorylated peptides, with serine residues representing the major site of phosphorylation. The motif-x analysis revealed the enrichment of [xxxpSPxxx], [RxxpSxxx] and [xxxpSDxxx] motifs, which are predicted phosphorylation sites for several kinases related to stress responses. Gene ontology enrichment revealed an overrepresentation of biological processes involved in embryonic development, showing that EC-related phosphoproteins (unique to EC and upaccumulated) were associated with stress responses, regulation of gene expression and epigenetic modifications. The NEC-related phosphoproteins (unique to NEC and downaccumulated) were associated with the translation process. In this sense, EC-related phosphoproteins described as potential regulators of abiotic stress tolerance in response to ABA-induced signals such as OSK3 (a catalytic subunit of SnRK1), ABF1, LEAs, REM4.1 and RD29Bs were identified. On the other hand, the NEC-related phosphoproteins EDR1 and PP2Ac-2 were negative regulators of ABA, suggesting a role of ABA in the acquisition of embryogenic competence linked to stress tolerance. Moreover, EC-related phosphoproteins associated with epigenetic modifications, such as HDA6, HDA19, and TPL, as well as those involved in embryo development, including ASIL1, M3KE1, MCM2, and GRV2, were identified as putative potential regulators of embryogenic competence. Our results provide novel data that may help elucidate the phosphorylation mechanisms controlling the activity, affinity and localization of specific proteins during somatic embryogenesis and suggest a role for these proteins in the hormonal signalling cascade leading to stress adaptation by reprogramming genetic expression.

Dataset Information

Ethylene-induced transcriptional and hormonal responses at the onset of sugarcane ripening.

Publications

Ethylene-induced transcriptional and hormonal responses at the onset of sugarcane ripening.

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