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Link to original content: https://pubmed.ncbi.nlm.nih.gov/31548423
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. 2019 Oct 8;116(41):20776-20785.
doi: 10.1073/pnas.1902747116. Epub 2019 Sep 23.

Maize sugary enhancer1 (se1) is a gene affecting endosperm starch metabolism

Xia Zhang  1   2 , Karl J Haro von Mogel  1 , Vai S Lor  1 , Candice N Hirsch  3 , Brian De Vries  1 , Heidi F Kaeppler  1 , William F Tracy  1 , Shawn M Kaeppler  4   5
Affiliations

Maize sugary enhancer1 (se1) is a gene affecting endosperm starch metabolism

Xia Zhang et al. Proc Natl Acad Sci U S A. .

Abstract

sugary enhancer1 (se1) is a naturally occurring mutant allele involved in starch metabolism in maize endosperm. It is a recessive modifier of sugary1 (su1) and commercially important in modern sweet corn breeding, but its molecular identity and mode of action remain unknown. Here, we developed a pair of near-isogenic lines, W822Gse (su1-ref/su1-ref se1/se1) and W822GSe (su1-ref/su1-ref Se1/Se1), that Mendelize the se1 phenotype in an su1-ref background. W822Gse kernels have lower starch and higher water soluble polysaccharide and sugars than W822GSe kernels. Using high-resolution genetic mapping, we found that wild-type Se1 is a gene Zm00001d007657 on chromosome 2 and a deletion of this gene causes the se1 phenotype. Comparative metabolic profiling of seed tissue between these 2 isolines revealed the remarkable difference in carbohydrate metabolism, with sucrose and maltose highly accumulated in the mutant. Se1 is predominantly expressed in the endosperm, with low expression in leaf and root tissues. Differential expression analysis identified genes enriched in both starch biosynthesis and degradation processes, indicating a pleiotropic regulatory effect of se1 Repressed expression of Se1 and Su1 in RNA interference-mediated transgenic maize validates that deletion of the gene identified as Se1 is a true causal gene responsible for the se1 phenotype. The findings contribute to our understanding of starch metabolism in cereal crops.

Keywords: maize; starch metabolism; sugary enhancer1; sugary1.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Se1 and se1 phenotypes in the mapping population and near isogenic lines and their carbohydrate analysis. (A) Ear derived from self-pollination of a W822GSe x W822Gse cross segregating smooth Se1 (homozygous [Se1/Se1/Se1] and heterozygous [Se1/Se1/se1 and Se1/se1/se1], expressed as the genotype of the triploid endosperm) and wrinkled se1 (homozygous [se1/se1/se1]) dry kernels. The purple and turquoise arrowheads indicate smooth and wrinkled kernels, respectively. (B) Individual smooth and wrinkled kernels viewed on a lightbox showing opaque and translucent phenotype, respectively. (C) W822GSe and W822Gse isolines homozygous for Se1 and se1 have uniformly smooth and wrinkled kernel phenotype, respectively. (D and E) Carbohydrate analysis of mature kernels at 45 d after pollination (DAP) (D) and immature kernels at 22 DAP (E) from W822GSe and W822Gse isolines. Frozen and lyophilized whole kernels from 3 ears of each genotype were analyzed for total sugar, water soluble polysaccharide (WSP), and starch content. Error bars are SD (SD, n = 3). *0.01 < P < 0.05; **P < 0.01. Se1 and se1 genotypes analyzed above are in the su1-ref/su1-ref genetic background.
Fig. 2.
Fig. 2.
Genetic mapping of Se1. (A) Location of Se1 region on chromosome 2 indicated by the red box near the distal end. (B) Locus zoom of the Se1 region in B73 showing the 1.26 Mb between the markers Agt1 and UMC1736. Mapping markers and the number of recombinant plants with the Se1 genotype from the mapping population are indicated by the vertical lines and associated numbers. (C) Locus zoom of the 24-kb region surrounding Se1 in B73, with gene models indicated by the blue and yellow bars. AC217415.3_FG004 (Se1) is renamed Zm00001d007657 in gene model set Zm00001d.2 for assembly version Zm-B73-REFERENCE-GRAMENE-4.0. (D) Mapping data from 3 proximal and 3 distal recombinants (identified on the left). Vertical lines indicate marker locations. The purple bar represents regions Se1/se1 genotypes, teal indicates se1/se1 genotype, and gray indicates unknown genotype between markers. The genotypes of recombinants at the Se1 locus were determined by sequencing. All recombinants shown and homozygous se1/se1 controls possessed the deletion indicated by the light blue box and dotted lines, and all other gene models were excluded by the markers used for fine mapping.
Fig. 3.
Fig. 3.
Metabolic changes associated with mutant allele se1. (A) Scores plot from principal component analysis (PCA) of GC-MS–based metabolic profile in the developing endosperm of Se1 and se1. PC1, principal component 1; PC3, principal component 3. Each point indicates a metabolite profile of a biological replicate (n = 4, except for se1-11) at each development stage (11 to 21 DAP at 2-d interval). (B) Heat map visualization of relative abundance of sugars and sugar phosphates in the developing endosperm of B73, Se1, and se1 (11 to 21 DAP at 2-d interval). Metabolite abundance was log transformed and auto-scaled (mean-centered and divided by the SD of each variable) to form virtual colors as presented in the color key. (C and D) Sucrose and maltose levels in the developing endosperm of B73, Se1, and se1. The normalized spectrum abundance as described in Materials and Methods was used to indicate the metabolite level. Se1 and se1 represent W822GSe and W822Gse isolines, respectively, which are in the su1-ref/su1-ref genetic background.
Fig. 4.
Fig. 4.
Differentially expressed genes (DEGs) in W822Gse and W822GSe and enriched gene ontology (GO) terms for DEGs associated with starch metabolism. (A) Venn diagram of DEGs (FDR < 5%, |fold change| ≥ 1.5) between W822Gse and W822GSe at 11, 15, and 19 DAP. The number in each circle represents the amount of genes up-regulated (italic and bold), down-regulated (underlined), or contraregulated (red) in W822Gse relative to W822GSe. (B) Significantly enriched GO categories associated with the down-regulated genes in W822Gse at 15 DAP. The left y axis indicates the number of DEGs enriched in a category; the right y axis shows the number of genes included in a category. (C) Heat map of DEGs involved in starch biosynthesis. Values of log2fold change (W822Gse vs. W822GSe) at 11, 15, and 19DAP were used for clustering.
Fig. 5.
Fig. 5.
Kernel traits and Se1 and Su1 expression in RNAi transgenic maize. (A) A representative ear of BC2-self kernels on an ear from a self-pollinated Se1Su1-RNAi BC2 progeny segregating for wrinkled kernels (red arrow). X represents self-pollinated. (B) Visualization of RFP and wrinkled kernel phenotype for individual kernels segregating in the ear shown in A using a Leica fluorescent dissecting microscope. +/+, RFP kernels exhibiting the wrinkled phenotype; +/−, kernels exhibiting only RFP signal; −/−, kernels showing no RFP or wrinkled kernel phenotype. (C) Analysis of Se1 and Su1 expression by semiquantitative RT-PCR in RNAi transgenic maize. Self-pollinated BC2 progeny kernels of 3 independent events for Se1Su1-RNAi and Su1-RNAi and 2 events for Se1-RNAi (designated by TG1, TG2, and TG3) were used for analysis. B73, W822GSe, and W822Gse were used as references. TG and NT represent transgenic positive and nontransgenic sibling kernels. Actin1 was used as an endogenous loading control. The expected amplicons of Se1, Su1, and Actin are 171, 234, and 230 bp, respectively. (D) Kernel maltose level in RNAi transgenic maize. Mean maltose content (n = 14) was determined in self-pollinated BC2 progeny kernels (20 DAP) of 3 independent events for Se1Su1-RNAi and Su1-RNAi and 2 events for Se1-RNAi (designated by TG1, TG2, and TG3). B73, W822GSe, and W822Gse were used as references. TG and NT represent transgenic positive and nontransgenic sibling kernels. ***P < 0.001; NS, not significant (t test).
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