Rice PCR1 influences grain weight and Zn accumulation in grains

Abstract

Proteins containing a placenta-specific 8 domain (PLAC8) function as major organ size regulators in Solanum lycopersicum and Zea may, and putative metal ion transporters in Arabidopsis thaliana, Oryza sativa and Brassica juncea. However, it is unknown how PLAC8 domain-containing proteins fulfill such diverse roles. Here, we found that plant cadmium resistance 1 (PCR1) influences both zinc (Zn) accumulation and grain weight in rice. OsPCR1 knockout and knockdown lines produced lighter grains than the wild type, while OsPCR1 overexpression lines produced heavier grains. Furthermore, the grains of OsPCR1 knockdown lines exhibited substantially higher Zn and lower cadmium (Cd) concentrations than the control, as did yeast heterologously expressing OsPCR1. Through sequence analysis, we showed that the amino acid sequence of japonica-type PCR1 was distinct from that of indica-type and wild rice accessions. This difference was correlated with distinct Zn-related phenotypes. Japonica-type PCR1 had a shorter N-terminus than did PCR1 in the other rice types, and yeast heterologously expressing japonica-type PCR1 was more sensitive to Zn than was yeast expressing indica-type PCR1. Furthermore, japonica-type grains accumulated less Zn than did indica-type grains. Our study suggests that rice PCR1 maintains metal ion homeostasis and grain weight and might have been selected for during domestication. Proteins containing a placenta-specific 8 (PLAC8) domain regulate cell growth and cancer cell development in animals, fruit weight (FW2.2) in tomato, and cell number (ZmCNRs) in maize, and as putative metal ion transporters (PCRs, plant cadmium resistance) in Arabidopsis, rice, and Indian mustard. However, it has not been demonstrated how PLAC8 domain-containing proteins fulfill such diverse functions. Here, we report that rice PCR1 regulates both the Zn contents of grains and grain weight. OsPCR1 knockout and knockdown lines produced lighter grains, while OsPCR1 overexpression lines produced heavier grains than the wild type. Furthermore, the Zn and Cd contents were altered in grains of the transgenic rice lines as well as in yeast cells heterologously expressing OsPCR1. Through PCR1 sequence analysis using different rice accessions collected from many countries, we found that the PCR1s in Japonica and Indica rice exhibited distinct amino acid sequences, and this difference was associated with Zn resistance and accumulation Japonica PCR1 enhanced Zn hypersensitivity in yeast, and Japonica rice contained less Zn in their grains than did Indica rice. Our functional study and genetic analysis suggests that rice PCR1 maintains metal ion homeostasis and grain weight and might have evolved during domestication. We believe that this discovery will give great interest to the readership of Plant Cell and Environment, as it provides clues as to how PLAC8 domain-containing proteins fulfill diverse functions.