Transcriptome and metabolome profiling provide insights into molecular mechanism of pseudostem elongation in banana

Abstract

Background: Banana plant height is an important trait for horticultural practices and semi-dwarf cultivars show better resistance to damages by wind and rain. However, the molecular mechanisms controlling the pseudostem height remain poorly understood. Herein, we studied the molecular changes in the pseudostem of a semi-dwarf banana mutant Aifen No. 1 (Musa spp. Pisang Awak sub-group ABB) as compared to its wild-type dwarf cultivar using a combined transcriptome and metabolome approach.

Results: A total of 127 differentially expressed genes and 48 differentially accumulated metabolites were detected between the mutant and its wild type. Metabolites belonging to amino acid and its derivatives, flavonoids, lignans, coumarins, organic acids, and phenolic acids were up-regulated in the mutant. The transcriptome analysis showed the differential regulation of genes related to the gibberellin pathway, auxin transport, cell elongation, and cell wall modification. Based on the regulation of gibberellin and associated pathway-related genes, we discussed the involvement of gibberellins in pseudostem elongation in the mutant banana. Genes and metabolites associated with cell wall were explored and their involvement in cell extension is discussed.

Conclusions: The results suggest that gibberellins and associated pathways are possibly developing the observed semi-dwarf pseudostem phenotype together with cell elongation and cell wall modification. The findings increase the understanding of the mechanisms underlying banana stem height and provide new clues for further dissection of specific gene functions.

Keywords: Auxin efflux carrier proteins; Banana Pseudostem; Dwarfism; Ethylene response factors; Gibberellins.

Fig. 1

a) Six-week old wild type and semi-dwarf mutant plants of Aifen No. 1. The second panel shows the pseudostems used for combined omics analysis and b) comparison of plant height

Fig. 2

a Discrete and overall degree of gene expression in the replicates of both WT and MT Aifen No. 1 banana pseudostems. b Scatter plot of 20 most enriched KEGG pathways between WT and MT Aifen No. 1 banana pseudostems. The degree of enrichment is shown by Rich factor, Q-value, and the number of genes enriched in each pathway

Fig. 3

qRT-PCR analysis of the five selected differentially expressed genes in WT and WT banana pseudostems

Fig. 4

a Top-10 up-accumulated (shown in red bars) and top-10 down-accumulated metabolites (shown in green bars) in WT vs MT Aifen No.1 banana pseudostem. b Scatter plot of 20 KEGG pathways between WT and MT Aifen No. 1 banana pseudostems to which the differentially accumulated metabolites were enriched. The degree of enrichment is shown by Rich factor, P-value, and the number of metabolites enriched in each pathway

Fig. 5

Joint analysis of DEGs and DAMs between WT and MT Aifen No. 1 banana pseudostems. a Joint KEGG enrichment p-value histogram, b Pearson correlation coefficient of DEGs and DAMs in WT vs MT banana pseudostem represented as a nine-quadrant diagram. Black dots = unchanged genes/metabolites, green dots = DAMs with unchanged genes, red dots = DEGs with unchanged metabolites, blue dots = DEGs and DAMs. The Pearson’s correlation coefficient is > 0.8 throughout the nine-quadrant graph

Fig. 6

Proposed model of the hormonal cross talk leading to the increase in pseudostem height in MT Aifen No. 1 banana. Red arrow indicates the up (↑) or down (↓) regulated genes and red stars indicate that a putative interaction exists