A Metal Chaperone Gene Regulates Rice Growth and Seed Development by Manganese Acquisition and Homeostasis

Abstract

Manganese (Mn) is a mineral element essential for plant growth and development. In agronomy reality, Mn deficiency or overload in crops disturbs metal homeostasis, photosynthesis, and many other biological processes. Mining genetic resources linking Mn acquisition and homeostasis is vitally important to help understand plant adaptation to Mn stress and breeding genetically improved crops for sustainable agriculture. Metallic chaperone (metallochaperone) is a class of family proteins playing an essential role in positive responses to metal and abiotic stresses. Here, we report a novel function of a metal chaperone gene OsHIPP56 in regulating Mn accumulation in rice (Oryza sativa) crops. OsHIPP56 was transcriptionally induced by excessive Mn stress but hardly by Mn deficiency. OsHIPP56-expression in a yeast Mn-sensitive mutant pmr1 rescued the Mn-defective phenotype by increasing Mn accumulation in cells. Knocking out OsHIPP56 by Crispr/cas9 protocol did not affect the growth and physiological responses of rice seedlings supplied with normal Mn concentration. However, excess Mn stress moderately retarded growth of the knockout plants compared with the wild-type. A life span field trial was conducted under natural conditions with the two rice varieties. Knocking out OsHIPP56 also distorted rice growth, leading to reduced plant height, stem elongation, panicle length, spikelet fertility, seed size, and grain yield. Mn concentrations in rice straw (leaves and stem/internodes), brown rice, and husk in cas9 plants were much lower than those in wild-type. This was particularly seen in the brown rice where the Mn concentrations in cas9 plants were reduced by 26.7–49.1% compared with the wild-type control. Overall, these lines of evidence point out that OsHIPP56 plays a primary role required for rice growth, seed development, and Mn acquisition.

A Golgi-Located Transmembrane Nine Protein Gene TMN11 Functions in Manganese/Cadmium Homeostasis and Regulates Growth and Seed Development in Rice

“…Deletion of PMR1 in the pmr1 mutant results in a Mn-hypersensitive phenotype with severely blocked cellular growth and an overaccumulation of Mn ions [ 24 ]. This model is widely used for testing Mn transport, detoxification, and accumulation [ 7 , 25 , 26 ]. Our studies showed that under excessive Mn supply conditions, the growth of mutant cells carrying the null gene ( pmr1 + pYES2) was significantly inhibited compared to that of the wild-type (BY4741 + pYES2) yeast ( Figure 5 A).…”

“…Local meteorological data recorded no abnormal rainfall, temperature, pest, or disease occurrences, etc. When the rice was totally ripened, all of the tissues and organs of the mature plants were separately harvested [ 7 ].…”

“…Survey and analysis of mature rice structures and grain yields were conducted using previously described methods [ 7 ]. Briefly, the ripening rice plants were collected from the field, and their tissues and organs were separately sampled and surveyed in the lab.…”

“…While excessive Mn in rice dampens metal homeostasis and many other biological processes, Cd overload in rice also blocks plant growth, reduces food quality, and causes multi-chronic diseases through the food chain [ 4 ]. Mining genetic resources related to Mn and Cd acquisition to better understand how rice plants deal with metal toxicity is needed to not only answer a fundamental scientific question, but it is needed to build up genetically improved varieties that can adapt to stress environments [ 6 , 7 ]. Over the last decades, a growing number of metal transporters relevant to Mn and/or Cd acquisition, translocation, and homeostasis, with potential applications in phytoremediation, have been identified in plants [ 8 , 9 , 10 ].…”