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OsAPL controls the nutrient transport systems in the leaf of rice (Oryza sativa L.)

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Abstract

Main conclusion

OsAPL positively controls the seedling growth and grain size in rice by targeting the plasma membrane H+-ATPase-encoding gene, OsRHA1, as well as drastically affects genes encoding H+-coupled secondary active transporters.

Abstract

Nutrient transport is a key component of both plant growth and environmental adaptation. Photosynthates and nutrients produced in the source organs (e.g., leaves) need to be transported to the sink organs (e.g., seeds). In rice, the unloading of nutrients occurs through apoplastic transport (i.e., across the membrane via transporters) and is dependent on the efficiency and number of transporters embedded in the cell membrane. However, the genetic mechanisms underlying the regulation of these transporters remain to be determined. Here we show that rice (Oryza sativa L., Kitaake) ALTERED PHLOEM DEVELOPMENT (OsAPL), homologous to a MYB family transcription factor promoting phloem development in Arabidopsis thaliana, regulates the number of transporters in rice. Overexpression of OsAPL leads to a 10% increase in grain yield at the heading stage. OsAPL acts as a transcriptional activator of OsRHA1, which encodes a subunit of the plasma membrane H+-ATPase (primary transporter). In addition, OsAPL strongly affects the expression of genes encoding H+-coupled secondary active transporters. Decreased expression of OsAPL leads to a decreased expression level of nutrient transporter genes. Taken together, our findings suggest the involvement of OsAPL in nutrients transport and crop yield accumulation in rice.

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Data availability statement

The raw transcriptome data generated and analyzed in this study are available in the Sequence Read Archive with the identifier PRJNA603205. The raw ChIP-sequencing data generated and analyzed in this study are available in the Sequence Read Archive with the identifier PRJNA603254.

Abbreviations

APL:

Altered phloem development

DAG:

Days after germination

DEG:

Differentially expressed genes

OE:

Overexpression

PM:

Plasma membrane

SWEET:

Sugars will eventually be exported transporters

TF:

Transcription factor

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Acknowledgements

This study was supported by grants from the Ministry of Agriculture and Rural Affairs of the Peoples’ Republic of China (2016ZX08009003-005). We would like to thank Dr. Dong Zhang (PlantTech Biotechnology Co., Ltd) for providing suggestions on the analysis of transcriptomic data and ChIP-seq data. Part of computational analyses are supported by the High-performance Computing Platform of Peking University, and we thank Dr. Chun Fan and Yin-Ping Ma for their assistance during the analysis.

Author information

Author notes

  1. Zhen Yan and Man-Yu Yang contributed equally.

Authors and Affiliations

  1. Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, No. 20 Nanxincun, Xiangshan, Beijing, 100093, China

    Zhen Yan, Man-Yu Yang, Biligen-Gaowa Zhao, Guo Li, Qing Chao & Bai-Chen Wang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Zhen Yan, Man-Yu Yang, Biligen-Gaowa Zhao, Guo Li, Qing Chao & Bai-Chen Wang

  3. The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100039, China

    Qing Chao & Bai-Chen Wang

  4. Peking-Tsinghua Center for Life Sciences (CLS), Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, China

    Feng Tian & Ge Gao

  5. Beijing Advanced Innovation Center for Genomics (ICG) and Biomedical Pioneering Innovation Center (BIOPIC), Center for Bioinformatics (CBI), and State Key Laboratory of Protein and Plant Gene Research at School of Life Sciences, Peking University, Beijing, 100871, China

    Feng Tian

  6. College of Life Sciences, National Demonstration Center for Experimental Biology Education, Sichuan University, Chengdu, 610064, China

    Zhen Yan

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  1. Zhen Yan
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Supplementary Information

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425_2022_3913_MOESM1_ESM.tif

Supplementary file1 Fig. S1 Schematic diagram of conserved domains in OsAPL and phylogenetic analysis of APL proteins in other species. a Schematic diagram of OsAPL. ATG and TAA, the start and termination codons, respectively. SANT, the ‘SWI3, ADA2, N-CoR and TFIIIB' DNA-binding domain. Myb-CC, the highly conserved LHEQLE sequence motif. b Alignment of APL proteins from selected species. ZosmaAPL, Zostera marina; SpAPL, Sphagnum fallax; PpAPL, Physcomitrella patens; MpAPL, Marchantia polymorpha; SvAPL, Setaria viridis; AtrAPL, Amborella trichopoda; OsAPL, Oryza sativa; ZmAPL, Zea mays; SbAPL, Sorghum bicolor; BdAPL, Brachypodium distachyon; AtAPL, Arabidopsis thaliana; PtAPL, Populus trichocarpa; BsAPL, Brachypodium stacei; PhAPL, Panicum hallii; GlymaAPL, Glycine max; MtAPL, Medicago truncatula; GoraiAPL, Gossypium raimondii and AhAPL, Arabidopsis halleri. The amino acid sequences from different species were retrieved from Phytozome 12.0 by searching for the keyword APL. c Phylogenetic tree of APL proteins from rice and 18 other species generated by MEGA 7.0. For each protein the species name and primary protein transcript is listed. (TIF 8323 KB)

425_2022_3913_MOESM2_ESM.tif

Supplementary file2 Fig. S2 APL sequence conservation. a Phylogenetic tree based on the protein sequences of APL and its orthologous genes (left). Schematic of the protein structures from 162 plant species, colored by amino acids are shown on the right. The SANT and Myb_CC domains are highlighted by black boxes. b The dN/dS for each codon in APL, as estimated by HYPHY48. The average dN/dS ratio is 0.48, indicating purifying selection. (TIF 14063 KB)

425_2022_3913_MOESM3_ESM.tif

Supplementary file3 Fig. S3 The negative control of in-situ hybridization and GUS staining in this study. Negative control of in-situ hybridization in leaf main veins (a), middle veins (b) and minor veins (c). Bars=20 μm (a) 10μm (b )and 2.5μm (c). d to f Negative control of GUS staining in leaf main veins (d), middle veins (e) and minor veins (f). Bars=20 μm (a) 10μm (b) and 2.5μm (c). (TIF 1514 KB)

425_2022_3913_MOESM4_ESM.tif

Supplementary file4 Fig. S4 Morphological analysis of inner epidermis cells of lemma in wild type and different OsAPL transgenic lines. a to c The morphology of inner epidermis cells of lemma of the wild type (WT), RNAi line 7 (RNAi7) and overexpression line 1 (OE1), respectively, at 15 days after pollination. Bars=40 μm. d and e Inner epidermis cell length (d) and width (e) for WT, RNAi7 and OE1.Values are shown as box plots (Student’s t-test, **P≤0.01, n=150). (TIF 6089 KB)

425_2022_3913_MOESM5_ESM.tif

Supplementary file5 Fig. S5 Histological analysis of endosperm at the grain-filling stage in wild type and different OsAPL transgenic lines. a to c The morphology of endosperm epidermis cells at 15 days after pollination in the wild type (WT), RNAi line 7 (RNAi7) and overexpression line 1 (OE1), respectively. Bars=40 μm. d and e Endosperm epidermis cell length (d) and width (e) for WT, RNAi7 and OE1. Values are shown as box plots (Student’s t-test, **P≤0.01, n=200). (TIF 3289 KB)

425_2022_3913_MOESM6_ESM.tif

Supplementary file6 Fig. S6 Functions of genes differentially expressed between OsAPL overexpression Line 1 and wild type at different developmental stages. a GO enrichment analysis of DEGs between wild type (WT) and AsAPL overexpression line 1 (OE1) identified in leaves at 7 days after germination. b and c GO enrichment analysis of DEGs between WT and OE1 identified in flag leaves and glumes, respectively, at 14 days after pollination. In a to c, GO terms associated with transport processes are highlighted in red. (TIF 13307 KB)

425_2022_3913_MOESM7_ESM.tif

Supplementary file7 Fig. S7 GO enrichment analysis of OsAPL target genes. Using an adjusted P-value <0.01 as the significance threshold, the majority of the target genes were classified into ten biological process, six cellular component and nine molecular function terms. Significantly enriched terms (FDR≤0.05) are shown. (TIF 2621 KB)

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Yan, Z., Yang, MY., Zhao, BG. et al. OsAPL controls the nutrient transport systems in the leaf of rice (Oryza sativa L.). Planta 256, 11 (2022). https://doi.org/10.1007/s00425-022-03913-3

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