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.

Effect of Exogenous Gibberellin, Paclobutrazol, Abscisic Acid, and Ethrel Application on Bulblet Development in Lycoris radiata

“…The reproductive efficiency of Lycoris species is mainly determined by their bulblet propagation efficiency ( Xu et al, 2020 ). Previous studies have shown that in Lycoris sprengeri and Lycoris aurea , bulblets are formed from the axils of the scales on the abaxial surface ( Ren et al, 2017 ), but in Lycoris radiata they are preferentially formed on the junctions of the innermost layers of scales and on the basal plate ( Xu et al, 2020 ). During formation, they initially present as axillary buds and gradually develop into bulblets.…”

“…In Lycoris species and other flowering species with bulbs, including Lilium and Hippeastrum , bulblet differentiation is mainly determined by carbohydrate metabolism in both bulblet and mother scales. Starch in the mother scale can be degraded into soluble sugars, which are transported to and promote bulblet formation and development through the starch synthesis in bulblets ( Zhang et al, 2013 ; Li et al, 2014 ; Ren et al, 2017 ; Xu et al, 2020 ). In previous studies, sucrose and starch metabolism were found to have a key function in bulblet development into a new bulb, which is controlled by a series of enzymes.…”

“…Sucrose can be cleaved by sucrose synthase (SUS; Angeles-Núñez and Tiessen, 2010 ), and glucose, one of the products, can be used as a direct substrate for starch synthesis under the control of three major starch synthesis-related enzymes: glucose-1-phosphate adenylyltransferase (AGPase), soluble starch synthase (SSS), and granule-bound SS (GBSS; Miao et al, 2016 ) – AGPase has the dominant promoting effect on the bulblet development process in Lycoris ( Xu et al, 2020 ). Previous studies have revealed that AGPase activity could be determined by genes encoding its large and small subunits, as the overexpression of these genes could enhance AGPase activity, resulting in the increase in starch content ( Li et al, 2011 ; Kang et al, 2013 ).…”

“…Previous studies have revealed that AGPase activity could be determined by genes encoding its large and small subunits, as the overexpression of these genes could enhance AGPase activity, resulting in the increase in starch content ( Li et al, 2011 ; Kang et al, 2013 ). We also proposed that the overexpression of genes encoding AGPase subunits through transgenic and other molecular biology approaches could lead to significant promotion of AGPase activity in Lycoris bulbs, which may result in higher proliferation efficiency of the bulblets ( Xu et al, 2020 ). However, because of the lack of a transformation system, it is currently not possible to improve the reproductive efficiency of Lycoris through transgenic approaches.…”

“…Previous research on Lilium suggested that increasing auxin levels while decreasing CK levels might be useful for promoting bulblet development, whereas increasing only CK levels could be used to promote bulblet formation ( Kumar et al, 2007 ; Tang et al, 2010 ). Our recent study on the bulblet development process in L. radiata indicated that endogenous auxin, CK, GA, brassinosteroids (BR), jasmonic acid (JA), and salicylic acid (SA) may have promoting effects on bulblet formation, whereas ABA and ethylene may have suppressing effects on bulblet formation ( Xu et al, 2020 ), but the effect of these hormones should be further verified by external application to test their suitability for regulating bulblet development in Lycoris .…”