MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction

Abstract

Sexual reproduction in flowering plants involves double fertilization, the union of two sperm from pollen with two sex cells in the female embryo sac. Modern plant breeders increasingly seek to circumvent this process to produce doubled haploid individuals, which derive from the chromosome-doubled cells of the haploid gametophyte. Doubled haploid production fixes recombinant haploid genomes in inbred lines, shaving years off the breeding process. Costly, genotype-dependent tissue culture methods are used in many crops, while seed-based in vivo doubled haploid systems are rare in nature and difficult to manage in breeding programmes. The multi-billion-dollar maize hybrid seed business, however, is supported by industrial doubled haploid pipelines using intraspecific crosses to in vivo haploid inducer males derived from Stock 6, first reported in 1959 (ref. 5), followed by colchicine treatment. Despite decades of use, the mode of action remains controversial. Here we establish, through fine mapping, genome sequencing, genetic complementation, and gene editing, that haploid induction in maize (Zea mays) is triggered by a frame-shift mutation in MATRILINEAL (MTL), a pollen-specific phospholipase, and that novel edits in MTL lead to a 6.7% haploid induction rate (the percentage of haploid progeny versus total progeny). Wild-type MTL protein localizes exclusively to sperm cytoplasm, and pollen RNA-sequence profiling identifies a suite of pollen-specific genes overexpressed during haploid induction, some of which may mediate the formation of haploid seed. These findings highlight the importance of male gamete cytoplasmic components to reproductive success and male genome transmittance. Given the conservation of MTL in the cereals, this discovery may enable development of in vivo haploid induction systems to accelerate breeding in crop plants.

Dissection of a major QTL qhir1 conferring maternal haploid induction ability in maize

“…When this publication was in production, three articles (Kelliher et al 2017; Gilles et al 2017; Liu et al 2017) were published about cloning the gene underlying qhir1 QTL that codes for a sperm specific phospholipase and triggers haploid induction.…”

Gametocidal Factor Transferred from Aegilops geniculata Roth Can Be Adapted for Large-Scale Chromosome Manipulations in Cereals

“…Doubled haploid (DH) breeding is the most productive way to incorporate new genes or loci for crop improvement. Plant breeders seek to bypass sexual reproduction, to produce DH individuals derived from the chromosome-doubled cells of the haploid gametophyte (Kelliher et al, 2017). The key role of DH production is a fixation of recombinant haploid genomes in inbred lines (Chang and Coe, 2009).…”

A Diallel Analysis of a Maize Donor Population Response to In Vivo Maternal Haploid Induction: I. Inducibility

“…The genome of the inducer is subsequently eliminated from the embryo, which becomes haploid, containing only the genome of the donor parent, which is a result of one meiotic recombination during egg cell development. The pollen-specific gene MATRILINEAL has been identified as the major gene affecting the ability of maternal inducer lines to induce haploid progeny (Kelliher et al, 2017); however, this does not provide evidence for either of the two hypotheses. Without production of a normal healthy endosperm, the survival of the seed would not be possible without special care.…”