Abstract

Imprinted genes display biased expression of paternal and maternal alleles and are only found in mammals and flowering plants. Compared to several hundred imprinted genes that are functionally characterized in mammals, very few imprinted genes were confirmed in plants and even fewer of them have been functionally investigated. Here, we report a new imprinted gene, NUWA, in plants. NUWA is an essential gene, because loss of its function resulted in reduced transmission through the female gametophyte and defective cell/nuclear proliferation in early Arabidopsis embryo and endosperm. NUWA is a maternally expressed imprinted gene, as only the maternal allele of NUWA is transcribed and translated from gametogenesis to the 16-cell globular embryo stage after fertilization, and the de novo transcription of the maternal allele of NUWA starts from the zygote stage. Different from other identified plant imprinted genes whose encoded proteins are mostly localized to the nucleus, the NUWA protein was localized to the mitochondria and was essential for mitochondria function. Our work uncovers a novel imprinted gene of a previously unidentified type, namely, a maternal-specific expressed nuclear gene with its encoded protein localizing to and controlling the function of the maternally inherited mitochondria. This reveals a unique mechanism of maternal control of the mitochondria and adds an extra layer of complexity to the regulation of nucleus-organelle coordination during early plant development.

Highlights

  • Genomic imprinting is a phenomenon in which somatic cells express some genes only from the maternal or paternal chromosome [1]

  • Mitochondrial Function Regulated by a Novel Imprinted Gene mitochondria

  • The discovery of NUWA reveals a unique mechanism of maternal control of mitochondrial function and adds an extra layer of complexity to nucleus-organelle coordination

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Summary

Introduction

Genomic imprinting is a phenomenon in which somatic cells express some genes only from the maternal or paternal chromosome [1]. Genes with parent-of-origin-specific allele-biased expression patterns are called imprinted genes [2,3]. Imprinted genes have only been discovered and confirmed in placental mammals and flowering plants and are thought to have evolved independently through convergent evolution in these two groups [4,5]. In mammals, imprinted genes are essential in embryonic development and placental development of the fetus and in sensory function and behavior in adults [9,10,11]. In plants, imprinted genes are involved in early development, and the loss-of-function of these genes can lead to seed-lethal phenotypes [2,3]

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