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Identification and characterization of genes involved in element transport through ionome screening in Oryza sativa

闞, 慢慢 東京大学 DOI:10.15083/0002004433

2022.06.22

概要

Introduction
The ionome is defined as the mineral nutrient and trace element composition of an organism and represents the inorganic component of cellular and organismal systems (Salt et al., 2008). Plants develop strategies to tightly maintain elements homeostasis through regulating processes including uptake, sequestration, translocation, distribution and regulation. Thus, elements accumulation in plants is a complex process regulated by a network of gene products. To gain insight how elements are taken up, sequestered, and translocated, ionome analysis is a helpful way to take elemental concentrations by combining with genetics. In recent years, high-throughput elements analysis, such as inductively coupled plasma mass spectrometry (ICP-MS) combined with genetics have identified genes regulating ionome.

In this study, to investigate elements transport in rice, I focused on ethyl methanesulfonate (EMS)- mutagenized Oryza sativa mutants isolated by ionome screening of brown rice in our laboratory. Through analyzing these mutants, I identified genes involved in Co and Ni transport and detoxification, and distribution of Zn and Cd in rice, respectively.

Chapter 1. OsFPN1 is required for Co and Ni detoxification in rice

In this chapter, through ionome screening, I utilized previously isolated an EMS-mutagenized mutant 1187_n, which exhibited increased Co and Ni in brown rice. To investigate the distribution of Co and Ni in 1187_n, Co and Ni in leaf and xylem sap were determined. High concentrations of Co and Ni were observed in leaf and xylem sap, indicating Co and Ni homeostasis was altered in 1187_n. In addition, the mutant showed sensitivity to high Co and Ni. These results suggest that the causal gene is responsible for both Co and Ni transport from root to shoot and required for high Co and Ni tolerance.

The mutant showed similar ionome phenotype to Arabidopsis thaliana ferroportin (FPN) mutant. Sequencing result of rice homologous gene, OsFPN1, showed that 1187_n has nucleotide substitution following amino acid substitution in OsFPN1. The mutated amino acid is highly conserved in plant and human homologs and predicted to function as metal binding site. To observe the cosegregation of the mutation and the phenotype, I determined Co and Ni concentrations and the genotype in F2 crosses between 1187_n and wild type. The result show that there is a correlation between them. Further, I established two CRISPR/Cas9 lines, and they exhibited increased Co and Ni concentrations in shoot. These data demonstrated that the causal gene responsible for the alteration of Co and Ni in 1187_n is OsFPN1.

To investigate the Co and Ni transport activity of OsFPN1, GFP-fused OsFPN1 (GFP-OsFPN1) was expressed in yeast. Heterologous expression of GFP-OsFPN1 increased sensitivity to high Co. Furthermore, the yeast expressing GFP-OsFPN1 accumulated low Co and Ni compared to that of empty vector. These results demonstrate that OsFPN1 is able to transport Co and Ni. To determine the subcellular localization, GFP-OsFPN1 was transiently expressed in protoplast prepared from leaf sheath. The fluorescence was observed as dot in cell. The GFP fluorescence was colocalized with Golgi marker protein, indicating OsFPN1 is localized to Golgi. Taken together, OsFPN1 is Golgilocalized Co and Ni transporter.

It has been reported that the function of Arabidopsis FPN2 is to prevent the transport of excess Co and Ni to shoot by sequestering them in root. To test if the OsFPN1 has similar function in rice, I grew wild type and mutant under different concentrations of Co and Ni, and Fe. In both wild type and the mutant, Co and Ni concentrations increased as Fe concentration in hydroponic culture decreased both in roots and shoots. However, the difference between wild type and the mutant became larger. This suggests OsFPN1 contributes to prevention of Co and Ni transport from root to shoot. Taken together, OsFPN1 is required for the Co and Ni tolerance especially under low Fe condition.

Co and Ni are contaminant of soil and inhibit the growth of plants. To test if overexpression of OsFPN1 confer the tolerance to rice, I grew rice under high Co or Ni condition. Overexpression of OsFPN1 exhibited dramatically longer shoot compared to wild-type Nipponbare under high Co condition, indicating OsFPN1 is useful gene to confer tolerance to these elements.

Chapter 2. Identification of novel allele of OsHMA2, a Zn and Cd transporter

In chapter 2, I utilized previously identified EMS-mutagenized mutant named 391_n, which exhibited decreased Zn in brown rice, through ionome screening. To investigate the distribution of Zn in 391_n, elements in shoot and xylem sap of 391_n were determined. Zn and Cd concentrations were reduced both in shoot and xylem sap, indicating that the causal gene is responsible for the shoot to root transport of these elements. To identify the gene responsible for the alteration of Zn and Cd concentrations in 391_n, 391_n was back crossed with wild type, and Zn and Cd concentrations were determined in F2 population. Zn and Cd concentrations were correlated with each other in F2 population, indicating that the same gene is responsible for the Zn and Cd alteration. To identify the gene, I used 15 plants of high and low Zn and Cd concentrations, respectively, for genetic mapping using next generation sequencer. The analysis showed that the causal gene was located at a region between 27217030 bp and 31042767 bp on chromosome 6. In this region, OsHMA2, a known Zn transporter, had nucleotide substitution following amino acid substitution. The mutation site is highly conserved among plants. The Tos17 mutants of OsHMA2 exhibited low Zn and Cd in shoot but inverse in root compared to wild type, which is similar to 391_n. These results suggest OsHMA2 is the causal gene of 391_n and is responsible for root to shoot transport of Zn and Cd. To investigate Zn distribution among leaves, Zn concentration in leaf blade were determined. Zn distribution of the mutant was different from that of wild type: in wild type, Zn concentration of flag leaf is higher than other old leaves, however, in 391_n, Zn concentration is similar among leaves. These results suggest that OsHMA2 is also involved in Zn distribution among leaves.

Summary
In this thesis, through the characterization of EMS-mutagenized Oryza sativa mutants isolated by ionome screening, two genes associated with elements transport were identified and characterized. In chapter 1, OsFPN1 was demonstrated to be responsible for Co and Ni transport and tolerance. In addition, I succeeded in establishing Co and Ni tolerance rice. In chapter 2, a novel allele of OsHMA2 was identified and is responsible for the root to shoot translocation of Zn and Cd and distribution among leaves.

Co is the beneficial element and Ni is the essential element for plant. However, to date, the mechanism of Co and Ni transport and detoxification in rice is unclear. Through the achievements of my thesis, I gain insight into how Co and Ni are transported in rice and established Co and Ni tolerance lines, which can be applicable for removing excess Co and Ni from high Co and Ni containing soil. In addition, I identified a novel OsHMA2 allele and illustrate the conserved glycine in the exon 6 of OsHMA2 is critical for the distribution of Zn and Cd.

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