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Changes in carbohydrate metabolism and endogenous hormone regulation during bulblet initiation and development in Lycoris radiata.

ABSTRACT: BACKGROUND:Lycoris species have great ornamental and medicinal values; however, their low regeneration efficiency seriously restricts their commercial production. Understanding the mechanism of bulblet propagation in this genus, which has remained underexplored to date, could provide a theoretical basis for improving the reproductive efficiency. Therefore, we studied the bulblet initiation and developmental processes in Lycoris radiata. RESULTS:We found that bulblets are formed on the junctions of the innermost layers of scales and the basal plate, and initially present as an axillary bud and gradually develop into a bulblet. We also determined the changes in carbohydrate and endogenous hormone contents during bulblet initiation and development, as well as the expression patterns of genes involved in carbohydrate metabolism and hormone biosynthesis and signaling through transcriptome analysis. Soluble sugars derived from starch degradation in the outer scales are transported to and promote bulblet initiation and development through starch synthesis in the inner scales. This process is mediated by several genes involved in carbohydrate metabolism, especially genes encoding ADP glucose pyrophosphorylase, a crucial starch synthesis enzyme. As for hormones, endogenous IAA, GA, and ABA content showed an increase and decrease during bulblet initiation and development, respectively, which were consistent with the expression patterns of genes involved in IAA, GA, and ABA synthesis and signal transduction. In addition, a decrease in ZR content may be down- and up-regulated by CK biosynthesis and degradation related genes, respectively, with increasing auxin content. Furthermore, expression levels of genes related to BR, JA, and SA biosynthesis were increased, while that of ethylene biosynthesis genes was decreased, which was also consistent with the expression patterns of their signal transduction genes. CONCLUSIONS:The present study provides insights into the effect of carbohydrate metabolism and endogenous hormone regulation on control of L. radiata bulblet initiation and development. Based on the results, we propose several suggestions to improve L. radiata propagation efficiency in production, which will provide directions for future research.

SUBMITTER: Xu J

PROVIDER: S-EPMC7183599 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Changes in carbohydrate metabolism and endogenous hormone regulation during bulblet initiation and development in Lycoris radiata.

Xu Junxu J Li Qingzhu Q Yang Liuyan L Li Xin X Wang Zhen Z Zhang Yongchun Y

BMC plant biology 20200425 1

<h4>Background</h4>Lycoris species have great ornamental and medicinal values; however, their low regeneration efficiency seriously restricts their commercial production. Understanding the mechanism of bulblet propagation in this genus, which has remained underexplored to date, could provide a theoretical basis for improving the reproductive efficiency. Therefore, we studied the bulblet initiation and developmental processes in Lycoris radiata.<h4>Results</h4>We found that bulblets are formed on ...[more]

PMID: 32334530

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Project description:Lycoris species have great ornamental and medicinal values; however, their low regeneration efficiency significantly restricts their commercial production. Exogenous hormone application is an effective way to promote bulblet development, but their effect on Lycoris radiata has not been verified to date. In the present study, we examined the effect of different exogenous hormones on bulblet development in L. radiata, and found that gibberellic acid (GA) significantly inhibited, whereas paclobutrazol (PBZ), abscisic acid (ABA), and ethrel promoted bulblet development, especially PBZ, a GA biosynthesis inhibitor. Furthermore, GA reduced endogenous cytokinin (CK) content, as well as the activities of carbohydrate metabolism enzymes, including sucrose synthase (SUS) and glucose-1-phosphate adenylyltransferase (AGPase), by downregulating the expression levels of LrSUS1, LrSUS2, and genes encoding AGPase large and small subunits. This resulted in the decrease in carbohydrate accumulation in the bulblets, thus hindering their development. PBZ had the opposite effect to GA on carbohydrate metabolism; it decreased endogenous GA15 and GA24, thereby promoting bulblet development. ABA promoted endogenous auxin content and the activities of starch synthesis enzymes, especially soluble starch synthase (SSS) and granule-bound SS (GBSS), through the up-regulation of the expression levels of LrSS1, LrSS2, and LrGBSS1 genes, which could also result in the accumulation of carbohydrates in the bulblets and promote their development. In addition, ethrel application partly promoted bulblet development by promoting endogenous CK content. Although the accumulation of carbohydrates and the activity of starch enzymes were increased by ethrel treatment, we hypothesized that the effect of ethrel on regulating carbohydrate metabolism may be indirect. Our results could provide a basis for improving the propagation efficiency of L. radiata for production, as well as propose some directions for future research.

Project description:Lycoris radiata belongs to the Amaryllidaceae family and is a bulbous plant native to South Korea, China, and Japan. Galantamine, a representative alkaloid of Amaryllidaceae plants, including L. radiata, exhibits selective and dominant acetylcholinesterase inhibition. In spite of the economic and officinal importance of L. radiata, the molecular biological and biochemical information on L. radiata is relatively deficient. Therefore, this study provides functional information of L. radiata, describe galantamine biosynthesis in the various organs, and provide transcriptomic and metabolic datasets to support elucidation of galantamine biosynthesis pathway in future studies. The results of studies conducted in duplicate revealed the presence of a total of 325,609 and 404,019 unigenes, acquired from 9,913,869,968 and 10,162,653,038 raw reads, respectively, after trimming the raw reads using CutAdapt, assembly using Trinity package, and clustering using CD-Hit-EST. All of the assembled unigenes were aligned to the public databases, including National Center for Biotechnology Information (NCBI) non-redundant protein (NR) and nucleotide (Nt) database, SWISS-PROT (UniProt) protein sequence data bank, The Arabidopsis Information Resource (TAIR), the Swiss-Prot protein database, Gene Ontology (GO), and Clusters of Orthologous Groups (COG) database to predict potential genes and provide their functional information. Based on our transcriptome data and published literatures, eight full-length cDNA clones encoding LrPAL2, LrPAL3, LrC4H2, LrC3H, LrTYDC2, LrNNR, LrN4OMT, and LrCYP96T genes, involved in galantamine biosynthesis, were identified in L. radiata. In order to investigate galantamine biosynthesis in different plant parts of L. radiata grown in a growth chamber, gene expression levels were measured through quantitative real-time polymerase chain reaction (qRT-PCR) analysis using these identified genes and galantamine levels were quantified by high-performance liquid chromatography (HPLC) analysis. The qRT-PCR data revealed high expression levels of LrNNR, LrN4OMT, and LrCYP96T in the bulbs, and, as expected, we observed higher amounts of galantamine in the bulbs than in the root and leaves. Additionally, a total of 40 hydrophilic metabolites were detected in the different organs using gas-chromatography coupled with time-of-flight mass spectrometry. In particular, a strong positive correlation between galantamine and sucrose, which provides energy for the secondary metabolite biosynthesis, was observed.

Project description:BackgroundThe formation and development of bulblets are crucial to the Lilium genus since these processes are closely related to carbohydrate metabolism, especially to starch and sucrose metabolism. However, little is known about the transcriptional regulation of both processes. To gain insight into carbohydrate-related genes involved in bulblet formation and development, we conducted comparative transcriptome profiling of Lilium davidii var. unicolor bulblets at 0 d, 15 d (bulblets emerged) and 35 d (bulblets formed a basic shape with three or four scales) after scale propagation.ResultsAnalysis of the transcriptome revealed that a total of 52,901 unigenes with an average sequence size of 630 bp were generated. Based on Clusters of Orthologous Groups (COG) analysis, 8% of the sequences were attributed to carbohydrate transport and metabolism. The results of KEGG pathway enrichment analysis showed that starch and sucrose metabolism constituted the predominant pathway among the three library pairs. The starch content in mother scales and bulblets decreased and increased, respectively, with almost the same trend as sucrose content. Gene expression analysis of the key enzymes in starch and sucrose metabolism suggested that sucrose synthase (SuSy) and invertase (INV), mainly hydrolyzing sucrose, presented higher gene expression in mother scales and bulblets at stages of bulblet appearance and enlargement, while sucrose phosphate synthase (SPS) showed higher expression in bulblets at morphogenesis. The enzymes involved in the starch synthetic direction such as ADPG pyrophosphorylase (AGPase), soluble starch synthase (SSS), starch branching enzyme (SBE) and granule-bound starch synthase (GBSS) showed a decreasing trend in mother scales and higher gene expression in bulblets at bulblet appearance and enlargement stages while the enzyme in the cleavage direction, starch de-branching enzyme (SDBE), showed higher gene expression in mother scales than in bulblets.ConclusionsAn extensive transcriptome analysis of three bulblet development stages contributes considerable novel information to our understanding of carbohydrate metabolism-related genes in Lilium at the transcriptional level, and demonstrates the fundamentality of carbohydrate metabolism in bulblet emergence and development at the molecular level. This could facilitate further investigation into the molecular mechanisms underlying these processes in lily and other related species.

Project description:Bulblet initiation, including adventitious bud initiation and bulblet formation, is a crucial process for lily and other bulbous flowers that are commercially propagated by vegetative means. Here, by a hybrid strategy combining Pacific Biosciences (PacBio) full-length sequencing and Illumina RNA sequencing (RNA-seq), high-quality transcripts of L. brownii (Lb) and its variety, L. brownii var. giganteum (Lbg), during in vitro bulblet initiation were obtained. A total of 53,576 and 65,050 high-quality non-redundant full-length transcripts of Lbg and Lb were generated, respectively. Morphological observation showed that Lbg possessed a stronger capacity to generate bulblets in vitro than Lb, and 1 mg L-1 2,4-dichlorophenoxyacetic acid (2,4-D) significantly increased bulblet regeneration rate in two lilies. Screening of differentially expressed transcripts (DETs) between different stages and Mfuzz analysis showed 0 DAT to 1 DAT was the crucial stage with the most complex transcriptional change, with carbohydrate metabolism pathway was significantly enriched. In addition, 6,218 and 8,965 DETs were screened between the 2,4-D-treated group and the control group in Lbg and Lb, respectively. 2,4-D application had evident effects on the expression of genes involved in auxin signaling pathway, such as TIRs, ARFs, Aux/IAAs, GH3s and SAURs. Then, we compared the expression profiles of crucial genes of carbohydrate metabolism between different stages and different treatments. SUSs, SUTs, TPSs, AGPLs, GBSSs and SSs showed significant responses during bulblet initiation. The expression of CWINs, SUTs and SWEETs were significantly upregulated by 2,4-D in two lilies. In addition, 2,4-D increased the expression of starch degradation genes (AMYs and BAMs) and inhibited starch synthesis genes (AGPLs, GBSSs and SSs). SBEs were significantly upregulated in Lbg but not in Lb. Significant co-expression was showed between genes involved in carbohydrate metabolism and auxin signaling, together with transcription factors such as bHLHs, MYBs, ERFs and C3Hs. This study indicates the coordinate regulation of bulblet initiation by carbohydrate metabolism and auxin signaling, serving as a basis for further studies on the molecular mechanism of bulblet initiation in lily and other bulbous flowers.

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Changes in carbohydrate metabolism and endogenous hormone regulation during bulblet initiation and development in Lycoris radiata.

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Changes in carbohydrate metabolism and endogenous hormone regulation during bulblet initiation and development in Lycoris radiata.

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