Identification, characterization, and cloning of Arabidopsis rhd1-4: a UDP-glucose-4-epimerase mutant that exhibits hypersusceptibility to the sugar beet cyst nematode and altered root ethylene responses

Cyst nematodes (genus Heterodera) constitute an economically important class of plant pathogens that induce the formation of a complex feeding site, i.e., a syncytium, within host plant roots. Cyst nematode-induced modulations in host cell gene expression and signal transduction, via the activity of nematode esophageal gland secretions, are likely required in order to bring about syncytium formation. However, the identities of these host genes and signaling pathways targeted by the nematode remain obscure. In an effort to identify host genes pertinent to successful cyst nematode parasitism, a forward genetics mutant screen was implemented based on the Arabidopsis thaliana-Heterodera schachtii (sugarbeet cyst nematode) compatible interaction. This screen yielded an H. schachtii hypersusceptible mutant that was later determined to be the fourth identified allele of the rhd1 (root hair defective) mutant. rhd1-4 is a recessive nuclear mutation that, in addition to H. schachtii hypersusceptibility, causes increased root hair elongation, decreased root length, and root epidermal cell bulging. We found that inhibition of ethylene synthesis or downstream ethylene signal transduction in rhd1-4 plants rescued the mutant phenotypes. The role of ethylene in mediating A. thaliana susceptibility to H. schachtii was further examined by assaying the susceptibilities of mutant genotypes that either over-produced ethylene or were unable to perceive or transduce an ethylene signal. These experiments revealed that ethylene positively regulates A. thaliana susceptibility to H. schachtii. Double mutant analyses involving rhd1-4 and known ethylene signal transduction mutants indicated that rhd1-4 hypersusceptibility to H. schachtii was likely mediated by increased root sensitivity to ethylene. Furthermore, we determined that RHD1 encodes a UDP-glucose-4-epimerase that is responsible for UDP-galactose synthesis and whose expression is negatively regulated by ethylene. UDP-galactose is required for proper cell wall and arabinogalactan protein synthesis, processes that previously have been shown to be altered in rhd1 mutant roots. In summary, we hypothesize that rhd1-4 hypersusceptibility to H. schachtii is mediated by an increased sensitivity of the root to ethylene that is caused by either aberrant cell wall or arabinogalactan protein synthesis. Our data also highlight the crucial role that the hormone ethylene plays in mediating host susceptibility to cyst nematodes