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. 2023 Aug 19;12(16):2995.
doi: 10.3390/plants12162995.

The Maize ZmBES1/BZR1-9 Transcription Factor Accelerates Flowering in Transgenic Arabidopsis and Rice

Yuan Liu  1 , Hongwanjun Zhang  1 , Wenqi Feng  1 , Xiaolong Lin  1 , Aijun Gao  1 , Yang Cao  1 , Qingqing Yang  1 , Yingge Wang  1 , Wanchen Li  1 , Fengling Fu  1 , Haoqiang Yu  1
Affiliations

The Maize ZmBES1/BZR1-9 Transcription Factor Accelerates Flowering in Transgenic Arabidopsis and Rice

Yuan Liu et al. Plants (Basel). .

Abstract

In model plants, the BRI1-EMS suppressor 1 (BES1)/brassinazole-resistant 1 (BZR1) transcription factors play vital roles in regulating growth, development, and stimuli response. However, the roles of maize ZmBES1/BZR1 members are largely unknown. In this research, the ZmBES1/BZR1-9 gene was ectopically expressed in Arabidopsis and rice for the phenotyping of flowering. We found that the complementation and overexpression of ZmBES1/BZR1-9 in bes1-D mutant and wild type Arabidopsis both resulted in early flowering that was about 10 days shorter than in the untransformed control under long-day conditions. In addition, there was no difference in the rosette leaf number between all transgenic lines and the control. Subsequently, the ZmBES1/BZR1-9 gene was overexpressed in rice. It was found that overexpression lines of rice exhibited early flowering with heading dates that were 8 days shorter compared with untransformed plants. Moreover, the results of RNA-seq and qRT-PCR showed that five flowering-regulated genes, namely At2-MMP, AtPCC1, AtMYB56, AtPELPK1, and AtPRP10, were significantly up-regulated in all complementary and overexpressing lines of Arabidopsis. Meanwhile, the results of RNA-seq showed that 69 and 33 differentially expressed genes (DEGs) were up- and down-regulated in transgenic rice, respectively. Four flowering-related genes, namely OsGA20OX1, OsCCR19, OsBTBN19, and OsRNS4 were significantly up-regulated in transgenic lines. To sum up, our findings demonstrate that ZmBES1/BZR1-9 is involved in controlling flowering and provide insights into further underlying roles of BES1/BZR1s in regulating growth and development in crops.

Keywords: BES1/BZR1; ectopic expression; flowering period; regulation; vegetative growth.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Identification of transgenic Arabidopsis lines. (a) PCR detection. (b) RT-PCR. OE9-1, 9-2, 9-3, 9-5, 9-10, and 9-14 represent homozygous lines overexpressing the ZmBES1/BZR1-9 gene in Arabidopsis. The 911 bp fragment of ZmBES1/BZR1-9 was amplified and detected by PCR (a) and RT-PCR (b), respectively. M, DNA 2000 standard consisting of a 2000, 1000, 750, 500, 250, and 100 bp ladder from top to bottom. WT, wild type. The 545 bp fragment of AtACTIN2 was amplified and used as a reference.
Figure 2
Figure 2
Screening of transgenic rice. (a) Antibiotic screening. (b) PCR amplification. (c) RT-PCR. R9-1, R9-2, R9-3, R9-4, and R9-5 mean transgenic rice lines expressing the ZmBES1/BZR1-9 gene. The 911 bp and 582 bp fragments of ZmBES1/BZR1-9 were amplified and detected by PCR and RT-PCR, respectively. M, DNA 2000 standard consisting of a 2000, 1000, 750, 500, 250, and 100 bp ladder from top to bottom. WT, wild type. The 629 bp fragment of the OsGAPDH gene was amplified and used as a reference.
Figure 3
Figure 3
The phenotype of complementary lines under LD conditions (14 h light/10 h dark). (a) Flowering phenotype. (b) Days at flowering. (c) Dynamic statistics of flowering time. (d) The number of rosette leaves. The seeds of each line were germinated and grown in growth chambers under LD conditions. The days from germination to flowering, the percentage of flowering plants over the same time period, and the total rosette leaf number were measured from 25 plants in each replicate. WT, wild type. bes1-D, untransformed mutant. L9-3 and L9-5 represent complementary lines of ZmBES1/BZR1-9 in the bes1-D mutant. * and ** represent p < 0.05 and p < 0.01, respectively.
Figure 4
Figure 4
The phenotype of overexpressed lines under LD conditions (14 h light/10 h dark). (a) Flowering phenotype. (b) Days at flowering. (c) Dynamic statistics of flowering time. (d) The number of rosette leaves. The seeds of each line were germinated and grown in growth chambers under LD conditions. The days from germination to flowering, the percentage of flowering plants over the same time period, and the total rosette leaf number were measured from 25 plants in each replicate. WT, wild type. OE9-2 and OE9-3 represent lines overexpressing ZmBES1/BZR1-9. * and ** represent p < 0.05 and p < 0.01, respectively.
Figure 5
Figure 5
The flowering phenotype of transgenic Arabidopsis under SD conditions. (a) The phenotype of complementary lines. (b) The phenotype of overexpressed lines. (c) The number of rosette leaves. L9-3 and L9-5 represent complementary lines. OE9-2 and OE9-3 represent overexpressing lines. bes1-D, mutant; WT, wild type.
Figure 6
Figure 6
The relative expression of flowering-related genes in complementary lines (a) and overexpressing lines (b). L9-3 and L9-5 represent complementary lines; OE9-2 and OE9-3 represent overexpressing lines. bes1-D, mutant; WT, wild type. AtACTIN2 was used as a reference. * and ** represent p < 0.05 and p < 0.01, respectively.
Figure 7
Figure 7
The flowering phenotype of transgenic rice under SD conditions. (a) Phenotype. (b) Statistics of heading date. The transgenic rice plants were grown in Sanya in winter from mid-Oct to mid-March under natural SD conditions with 9.5–12h light. The values represent means ± SEs from three biological replicates. R9-1 and R9-5 represent transgenic lines. WT, wild type. ** represents p < 0.01.
Figure 8
Figure 8
DEGs of transgenic rice with ZmBES1/BZR1-9 gene compared with WT. (a) The common DEGs shared by R9−1 and R9−5. (b) GO analysis of common DEGs. (c) The relative expression level of flowering-related genes. R9−1 and R9−5 represent transgenic lines. WT, wild type. * and ** represent p < 0.05 and p < 0.01, respectively.
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