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. 2023 Oct 18:14:1259561.
doi: 10.3389/fpls.2023.1259561. eCollection 2023.

Comparative metabolomics analysis reveals dynamic changes in carbohydrate profiles of corms during the "relay growth" of konjac (Amorphophallus muelleri)

Ying Qi  1 , Penghua Gao  1 , Shaowu Yang  1 , Lifang Li  1 , Yanguo Ke  1 , Huanyu Wei  1 , Feiyan Huang  1 , Lei Yu  1
Affiliations

Comparative metabolomics analysis reveals dynamic changes in carbohydrate profiles of corms during the "relay growth" of konjac (Amorphophallus muelleri)

Ying Qi et al. Front Plant Sci. .

Abstract

The type and content of carbohydrates in konjac corms are an essential factors in determining the quality of konjac; however, the pattern of carbohydrate changes and the mechanism regulating the development of mother and daughter corms in the "relay growth" process of Amorphophallus muelleri remain unclear. This study aimed to investigate changes in corm carbohydrates during the growth cycle of A. muelleri and to compare the carbohydrate composition and the expression of related genes between mother and daughter corms. Integrated metabolome and RNA-seq analyses identified 37 differential metabolites as well as 8074 genes that were differentially expressed between mother and daughter corms, the majority of which were involved in starch and sucrose metabolism. More than 80% of the differential metabolites, including sucrose and starch, tended to accumulate in the mother corms; however, konjac glucomannan (KGM), as one of the most important carbohydrates and its major component of the corm, accumulated in higher amounts in the daughter corms. In addition, the expression of invertase and alpha-amylase that promote the breakdown of sucrose and starch was 351.78- and 15.63-fold higher, respectively, in the daughter corm, whereas that of the starch synthesis gene AkWAXY was only 0.096 times as high as in the mother corms. Furthermore, the level of cellulose synthase-like protein G, which promotes KGM synthesis, was 3.85 times higher in daughter corms compared to mother corms. Thus, we inferred that the daughter and mother corms had two distinct carbohydrate utilization strategies. This study provides insights into temporal changes in carbohydrates during the growth cycle of A. muelleri.

Keywords: Amorphophallus muelleri; carbohydrates; corms turnover; konjac glucomannan; starch; sucrose.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
(A) A diagram illustrating the growth cycle and growth traits of A muelleri. Eighteen samples from six key developmental stages were collected for metabolic profiling and RNA-seq at the stages indicated. DPS represents the number of days post sprouting. (B-D) Growth characteristics of A muelleri measured in this study. The axis indicates the sample harvest date. The changes in fresh weight of corms (B) and leaves (C), and plant height (D) of A muelleri during the growth cycle are shown. D, dormant corms; B, bud sprouting stage; L, first leaf maturation stage; SB, second bud sprouting stage; SL, second leaf maturation stage; ST, lodging period. Each data point represents the mean ± SE (n ≥ 6). The different letters above the bars indicate significant differences between developmental periods (P<0.05; based on One-way ANOVA followed by a post-hoc Tukey’s test).
Figure 2
Figure 2
RT-qPCR analysis of genes involved in starch, sucrose and KGM biosynthesis compared between mother and daughter corms of A. muelleri. The data indicate mean values ± standard deviation of three biological replicates. Asterisks indicate statistical significance using Student’s t test (*: P< 0.05; **: P< 0.01; ****: P< 0.0001). The last graph is the Pearson correlation between the RNA-seq and the RT-qPCR.
Figure 3
Figure 3
Differential metabolite analysis between mother and daughter corms. (A) Overview of the 874 metabolites found in corms, and their classification into classes. (B) PCA analysis of corm samples at each developmental stage. (C, D) Volcano map of differential metabolites between mother and daughter corms. (E) The common differential metabolites of the mother corm at bud emergence and leaf maturation compared to the corresponding period of the daughter corm. D, dormant corms; B, bud sprouting stage; L, first leaf maturation stage; SB, second bud sprouting stage; SL, second leaf maturation stage; ST, lodging period.
Figure 4
Figure 4
Heat maps showing (A) the clustering of carbohydrates and (B) correlation analysis with other differential metabolites between daughter and mother corms.
Figure 5
Figure 5
KEGG pathway enrichment analysis for (A, B) differential metabolites and (C, D) differentially expressed genes between daughter and mother corms of A muelleri. B, bud sprouting stage; L, first leaf maturation stage; SB, second bud sprouting stage; SL, second leaf maturation stage.
Figure 6
Figure 6
Comparison of the major carbohydrates and genes involved in starch, sucrose, and glucomannan metabolism pathways compared between daughter and mother corms. Changes in transcript levels are indicated by color codes. Red shows upregulated, and blue indicates downregulated gene expression (using FPKM values) in daughter corms at the second leaf maturity period (SL) compared to mother corms at the first leaf maturity period (L). The values of the fold change (SL vs. L) are log2 scaled. The pathways connecting sucrose, starch and glucomannan are shown. Dash lines represent speculative pathways. The bar charts show the changes in the carbohydrates content of daughter and mother corms at different developmental stages. The values represent means ± SE and are fold change in content of daughter corms compared to the content in mother corms at the dormant stage (D). Asterisks indicate statistical significance using One-way ANOVA with Tukey test (*: P< 0.05; **: P< 0.01; ***: P< 0.001). D, dormant corms; B, bud sprouting stage; L, first leaf maturation stage; SB, second bud sprouting stage; SL, second leaf maturation stage; ST, lodging period; SBE, starch branching enzyme; WAXY, granule-bound starch synthase; SS, starch synthase; AGPS, ADP-glucose pyrophosphorylase; AGPP, Nucleotidyl transferase PGM, phosphoglucomutase; PGI, glucose-6-phosphate isomerase; PMI, mannose-6-phosphate isomerase; PMM, phosphomannomutase; GMPP, GDP-mannose pyrophosphorylase; MSR, mannan-synthesis related; CSLG, cellulose synthase-like protein G; AMY, alpha-amylase; MP, maltose phosphorylase; G1PG, glucose-1-phosphate guanylyl transferase; Sus, Sucrose synthase; INV, invertase; SPP, sucrose-phosphatase; SPS, sucrose-phosphate synthase; UGP, UTP-glucose-1-phosphate uridylyltransferase; HXK, hexokinase.
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Grants and funding

The authors declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by Yunnan Fundamental Research Projects (NO. 202101BA070001-163), Yunnan Education Department Reserch Project (No. 2022J0644), Yunnan Province Youth Talent Support Program (No. 202101AU070047), Yunnan Provincial Science and Technology Department (No. 202301AT070055).

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