Molecular Foundations of Reproductive Lethality in Arabidopsis thaliana

Abstract

The SeedGenes database (www.seedgenes.org) contains information on more than 400 genes required for embryo development in Arabidopsis. Many of these EMBRYO-DEFECTIVE (EMB) genes encode proteins with an essential function required throughout the life cycle. This raises a fundamental question. Why does elimination of an essential gene in Arabidopsis often result in embryo lethality rather than gametophyte lethality? In other words, how do mutant (emb) gametophytes survive and participate in fertilization when an essential cellular function is disrupted? Furthermore, why do some mutant embryos proceed further in development than others? To address these questions, we first established a curated dataset of genes required for gametophyte development in Arabidopsis based on information extracted from the literature. This provided a basis for comparison with EMB genes obtained from the SeedGenes dataset. We also identified genes that exhibited both embryo and gametophyte defects when disrupted by a loss-of-function mutation. We then evaluated the relationship between mutant phenotype, gene redundancy, mutant allele strength, gene expression pattern, protein function, and intracellular protein localization to determine what factors influence the phenotypes of lethal mutants in Arabidopsis. After removing cases where continued development potentially resulted from gene redundancy or residual function of a weak mutant allele, we identified numerous examples of viable mutant (emb) gametophytes that required further explanation. We propose that the presence of gene products derived from transcription in diploid (heterozygous) sporocytes often enables mutant gametophytes to survive the loss of an essential gene in Arabidopsis. Whether gene disruption results in embryo or gametophyte lethality therefore depends in part on the ability of residual, parental gene products to support gametophyte development. We also highlight here 70 preglobular embryo mutants with a zygotic pattern of inheritance, which provide valuable insights into the maternal-to-zygotic transition in Arabidopsis and the timing of paternal gene activation during embryo development.

A Comprehensive Dataset of Genes with a Loss-of-Function Mutant Phenotype in Arabidopsis

“…For protein function classification, we utilized a system (Supplemental Table S3) developed for past work on mutant phenotypes in Arabidopsis (Meinke et al, 2003;Bryant et al, 2011;Muralla et al, 2011). To streamline this effort and facilitate comparisons of greatest interest, we limited function assignments to unique genes, essential seed and gametophyte genes, and proteins localized to chloroplasts and mitochondria.…”

“…A recent comparison of functions associated with defects in embryo and gametophyte development revealed that although interfering with DNA replication and RNA modification typically disrupts embryo rather than gametophyte development, and blocking cytosolic translation often leads to gametophyte defects, extensive overlap exists between protein functions required for embryo and gametophyte development (Muralla et al, 2011). Therefore, one cannot explain the difference between embryo and gametophyte mutants on the basis of protein function alone.…”

“…Whether eliminating an essential function results in embryo, gametophyte, or seedling lethality, however, can be difficult to predict. For instance, interfering with amino acid biosynthesis in Arabidopsis often leads to embryo lethality, but for species with long pollen tubes or haploid spores with reduced contributions from parental sporocytes, the consequence might be gametophyte lethality instead (Muralla et al, 2011). In other cases, genetic redundancy may prolong the growth of homozygotes until the seedling stage.…”

“…Additional updates were obtained from a recent publication on embryo and gametophyte essentials of Arabidopsis (Muralla et al, 2011). We classified essential genes as being required for early development or survival.…”

The ArabidopsisTUMOR PRONE5Gene Encodes an Acetylornithine Aminotransferase Required for Arginine Biosynthesis and Root Meristem Maintenance in Blue Light

“…Meiotic drift, as indicated by reduced transmission frequencies of the tup5-2 and tup5-3 insertion alleles in reciprocal crosses with the wild type, is likely due to a dysfunction of ovules and pollen grains carrying this genotype. The reduced fitness of gametes carrying a TUP5 null allele indicates that they are not exclusively cross-fed from surrounding tissues but need a certain degree of Arg autotrophy (Muralla et al, 2011). However, survival of some gametes also shows that maternal tissue ensures at least limited Arg supply to ovules and pollen grains.…”