Ethylene-mediated improvement in sucrose accumulation in ripening sugarcane involves increased sink strength

Abstract

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 acidand 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.

Enhanced Activity of Genes Associated With Photosynthesis, Phytohormone Metabolism and Cell Wall Synthesis Is Involved in Gibberellin-Mediated Sugarcane Internode Growth

“…In broad bean, soybean, and populous, GA promoted photosynthesis (Yuan and Xu, 2001;Tian et al, 2016), while in Plantago, the external application of GA, decreased the rate of photosynthesis (Dijkstra et al, 1990). In our study, the gene expression of CAB1, CAB7, and LHCB5, was higher in G2 and G3 than in G1, which indicated that GA treatment may have a positive effect on sugarcane photosynthesis including in CAB, a key chlorophyll biosynthesis gene (Chen et al, 2019). The increased expression of the genes in these pathways might be related to high growth activities of GA3-treated sugarcane, which enhances photosynthesis.…”

“…Sugarcane is a major agricultural crop in China, which as a country provides ∼80% of sugar produced globally (Chen et al, 2019), the second largest bioenergy crop in the world (Tomes et al, 2011). Sucrose is stored in the sugarcane stem and shoot height is an important determinant of sugar yield (Spaunhorst et al, 2019).…”

The sugarcane and sorghum kinomes: insights into evolutionary expansion and diversification

“…In Sbi, the LRR family has broadly been linked with the response to several types of stress (Kawahigashi et al, 2011;Azzouz-Olden et al, 2020;Filiz and Kurt, 2020), playing roles related to signal transduction in response to extracellular signals (Azzouz-Olden et al, 2020;Dhaka et al, 2020;Vikal et al, 2020), pollen development (Dhaka et al, 2020), metabolism, and chaperone functions (Vikal et al, 2020). In Ssp, in addition to its association with defense response processes (Xu et al, 2018;Yang et al, 2019), this family has already been associated with hormone metabolism (Chen et al, 2019), cellulose and lignin biosynthesis (Kasirajan et al, 2018), and sucrose synthesis (Vicentini et al, 2009).…”

Sugarcane Omics: An Update on the Current Status of Research and Crop Improvement

“…Similarly, the observed increase in phosphoenolpyruvate carboxylase (PEPC) gene expression supports the fact that higher sink demand results in a greater photosynthetic rate and thus affects the source activity. SPS was found to be active at the initial stages of sugarcane development, signifying its vital role in sucrose synthesis [126,144].…”