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. 2021 Dec 15;22(12):1002-1021.
doi: 10.1631/jzus.B2100174.

Effects of gibberellin priming on seedling emergence and transcripts involved in mesocotyl elongation in rice under deep direct-seeding conditions

Ya Wang  1 , Yuetao Wang  1 , Ruifang Yang  2 , Fuhua Wang  1 , Jing Fu  1 , Wenbo Yang  1 , Tao Bai  1 , Shengxuan Wang  1 , Haiqing Yin  3
Affiliations

Effects of gibberellin priming on seedling emergence and transcripts involved in mesocotyl elongation in rice under deep direct-seeding conditions

Ya Wang et al. J Zhejiang Univ Sci B. .

Abstract

Mesocotyl elongation is a key trait influencing seedling emergence and establishment in direct-seeding rice cultivation. The phytohormone gibberellin (GA) has positive effects on mesocotyl elongation in rice. However, the physiological and molecular basis underlying the regulation of mesocotyl elongation mediated by GA priming under deep-sowing conditions remains largely unclear. In the present study, we performed a physiological and comprehensive transcriptomic analysis of the function of GA priming in mesocotyl elongation and seedling emergence using a direct-seeding japonica rice cultivar ZH10 at a 5-cm sowing depth. Physiological experiments indicated that GA priming significantly improved rice seedling emergence by increasing the activity of starch-metabolizing enzymes and compatible solute content to supply the energy essential for subsequent development. Transcriptomic analysis revealed 7074 differentially expressed genes (false discovery rate of <0.05, |log2(fold change)| of ≥1) after GA priming. Furthermore, gene ontology (GO) and Kyoto encyclopedia of genes and genomes (KEGG) enrichment analyses revealed that genes associated with transcriptional regulation, plant hormone biosynthesis or signaling, and starch and sucrose metabolism were critical for GA-mediated promotion of rice mesocotyl elongation. Further analyses showed that the expression of the transcription factor (TF) genes (v-myb avian myeloblastosis viral oncogene homolog (MYB) alternative splicing 1 (MYBAS1), phytochrome-interacting factors 1 (PIF1), Oryza sativa teosinte branched 1/cycloidea/proliferating cell factor 5 (OsTCP5), slender 1 (SLN1), and mini zinc finger 1 (MIF1)), plant hormone biosynthesis or signaling genes (brassinazole-resistant 1 (BZR1), ent-kaurenoic acid oxidase-like (KAO), GRETCHEN HAGEN 3.2 (GH3.2), and small auxin up RNA 36 (SAUR36)), and starch and sucrose metabolism genes (α-amylases (AMY2A and AMY1.4)) was highly correlated with the mesocotyl elongation and deep-sowing tolerance response. These results enhance our understanding of how nutrient metabolism-related substances and genes regulate rice mesocotyl elongation. This may facilitate future studies on related genes and the development of novel rice varieties tolerant to deep sowing.

Keywords: Deep sowing; Direct-seeding; Gibberellin; Mesocotyl; Rice (Oryza sativa L.); Transcriptomic analysis.

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Figures

Fig. 1
Fig. 1. Phenotypic and physiological assays of ZH10 seedlings under conditions of GAPT (0), GAPT (10), and GAPT (50). (a) Mesocotyl length of ZH10 seedlings under conditions of GAPT (0), GAPT (10), and GAPT (50) 10 d after sowing at the 5-cm sowing depth. (b‒e) Mesocotyl length (b), α‍-amylase activity (c), β-amylase activity (d), and soluble sugar content (e) of ZH10 materials under conditions of GAPT (0), GAPT (10), and GAPT (50) 1, 3, 5, 7, and 10 d after sowing at the 5-cm sowing depth. GAPT (0), priming treatment with 0 mg/L GA3; GAPT (10), priming treatment with 10 mg/L GA3; GAPT (50), priming treatment with 50 mg/L GA3. Values are shown as mean±standard deviation (SD) of three biological replicates. Different letters on columns indicate significant differences among samples with different treatments at the same time point at P<0.05, according to Duncan's test. GA3, gibberellin A3; FW, fresh weight.
Fig. 2
Fig. 2. Comparative analysis of transcriptional changes in rice mesocotyls in response to different GAPT concentrations. (a) Number of DEGs in three different comparisons. (b) Venn diagram showing the distribution of the identified DEGs with more than two-fold changes as well as FDR values less than 0.05 for at least one out of three different comparisons. GAPT (0), priming treatment with 0 mg/L GA3; GAPT (10), priming treatment with 10 mg/L GA3; GAPT (50), priming treatment with 50 mg/L GA3. GA3, gibberellin A3; FDR, false discovery rate; DEG, differentially expressed gene.
Fig. 3
Fig. 3. KEGG pathway enrichment analysis of the effect of GAPT (10) (a) and GAPT (50) (b) on rice mesocotyls under deep-sowing conditions. GAPT (0), priming treatment with 0 mg/L GA3; GAPT (10), priming treatment with 10 mg/L GA3; GAPT (50), priming treatment with 50 mg/L GA3. Pathways with an FDR value less than 0.05 are shown. ***, **, and * indicate FDR values lower than 0.001, 0.01, and 0.05, respectively. KEGG, Kyoto encyclopedia of genes and genomes; GA3, gibberellin A3; FDR, false discovery rate.
Fig. 4
Fig. 4. Expression analyses of transcription factors in mesocotyls after GAPT. (a) Number of transcription factors (TFs) that were differentially expressed in two comparisons; (b) Venn diagram showing the differentially expressed TFs that were commonly detected in the two comparisons; (c) Expression trends of four TFs (MYBAS1, OsTCP5, SLN1, and PIF1) in rice mesocotyls under different GAPT concentrations. GAPT (0), priming treatment with 0 mg/L GA3; GAPT (10), priming treatment with 10 mg/L GA3; GAPT (50), priming treatment with 50 mg/L GA3. For each treatment, the gene expression levels are shown as FPKM values by mean±standard deviation (SD) of three biological replicates. Different lowercase letters indicate significant differences among samples under different treatments at P<0.05, according to Duncan's test. MYBAS1, v-myb avian myeloblastosis viral oncogene homolog (MYB) alternative splicing 1; OsTCP5, Oryza sativa teosinte branched 1/cycloidea/proliferating cell factor 5; SLN1, slender 1; PIF1, phytochrome-interacting factor 1; GA3, gibberellin A3; FPKM, fragments per kilobase of exon per million mapped read.
Fig. 5
Fig. 5. Expression profiles of some focused DEGs related to phytohormone signaling or synthesis in response to GAPT under deep sowing conditions. The DEGs used here met three criteria: FDR<0.05, |log2(fold change)|≥1, and average FPKM>0.2, as this figure shows. Red and blue colors depict up- and down-regulation, respectively. The scale shows log2(fold change). ABA, abscisic acid; DEG, differentially expressed gene; GAPT, priming treatment with gibberellin A3 (GA3); FDR, false discovery rate; FPKM, fragments per kilobase of exon per million mapped read.
Fig. 5
Fig. 5. Expression profiles of some focused DEGs related to phytohormone signaling or synthesis in response to GAPT under deep sowing conditions. The DEGs used here met three criteria: FDR<0.05, |log2(fold change)|≥1, and average FPKM>0.2, as this figure shows. Red and blue colors depict up- and down-regulation, respectively. The scale shows log2(fold change). ABA, abscisic acid; DEG, differentially expressed gene; GAPT, priming treatment with gibberellin A3 (GA3); FDR, false discovery rate; FPKM, fragments per kilobase of exon per million mapped read.
Fig. 6
Fig. 6. Expression profiles of some focused DEGs related to starch and sucrose metabolisms in response to GAPT under deep-sowing conditions. The DEGs used here met three criteria: FDR<0.05, |log2(fold change)|≥1, and average FPKM>0.2, as this figure shows. Red and blue colors depict up- and down-regulation, respectively. The scale shows log2(fold change). DEG, differentially expressed gene; GAPT, priming treatment with gibberellin A3 (GA3); FDR, false discovery rate; FPKM, fragments per kilobase of exon per million mapped read.
Fig. 7
Fig. 7. Expression trends of positive (a) and negative (b) regulators potentially associated with mesocotyl elongation at different sowing depths. Values are shown as mean±standard deviation (SD) of three biological replicates. Different letters on columns represent significant differences among samples under different sowing depths at P<0.05 based on Duncan's test. dRn, delta normalized reporter; MYBAS1, v-myb avian myeloblastosis viral oncogene homolog (MYB) alternative splicing 1; PIF1, phytochrome-interacting factors 1; BZR1, brassinazole-resistant 1; KAO, ent-kaurenoic acid oxidase-like; GH3.2, GRETCHEN HAGEN 3.2; AMY, amylase; OsTCP5, Oryza sativa teosinte branched 1/cycloidea/proliferating cell factor 5; SLN1, slender 1; SAUR36, small auxin-up RNA 36; MIF1, mini zinc finger 1.
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