Untangling sex determination in Bursaphelenchus nematodes

Sex and sexual characteristics are key aspects of an organism’s life and are determined by a biological process known as sex determination. These ever-changing mechanisms are broadly categorized by the type of “switch” that triggers them. Genetic sex determination depends on sex chromosomes, such as X and Y chromosomes in human beings, while environmental sex determination depends on factors such as temperature and the local male-female ratio. Although most sex determination mechanisms are genetic or environmental, a third type of sex determination, which depends on completely random factors, also exists. This, however, has not been fully explored.

The sex determination mechanism of Caenorhabditis elegans, a species of nematode, or our common roundworm, is one of the best understood aspects of its biology. In his case, embryos with two X chromosomes, or XX embryos, develop into hermaphrodites, while XO embryos, which have one sex chromosome – the X chromosome – develop into males. Several nematode species have a sex determination mechanism similar to that of C. elegans. Interestingly, however, some nematode species also rely on the XX/XY system for sex determination, along with X and Y types of sex chromosomes, as well as environmental factors. Unfortunately, the mechanisms that cause this variance in sex determination between nematode species have remained a mystery until now.

Recently, a group of researchers led by Associate Professor Ryoji Shinya of Meiji University, Japan, Professor Paul Sternberg of California Institute of Technology, USA, and Associate Professor Taisei Kikuchi of Miyazaki University, in Japan, conducted a study to understand sex determination. in two species of nematodes, Bursaphelenchus xylophilus and Bursaphelenchus okinawaensis. Dr. Shinya’s team has a long history of working with nematode research. In this new study, they conducted a genome-wide sex-specific comparative analysis to determine the initial trigger for sex determination in the two species of Bursaphelenchus, and a genetic screening to determine the genetic cascade that followed the trigger.

In their study published in Nature Communication, the researchers report that there is no difference in the number of chromosomes, or genome, between males and females in B. xylophilus and between males and hermaphrodites in B. okinawaensis. This suggests that these sexes in both nematode species have identical genomes and no sex chromosomes. Thus, sex determination in these species must be through non-genetic mechanisms.

To investigate this further, the team conducted an analysis to determine whether environmental factors such as temperature, nutrient availability and population density influenced sex determination in these organisms. They observed that these factors had a minimal effect on sex determination in larvae of these species and that none of the larvae turned into males.

Considering that the offspring produced by selfing in B. okinawaensis are essentially isogenic clones, it is clear that genetic differences are not necessary for sex determination in B. okinawaensis. Moreover, even under fixed environmental conditions, genetically identical individuals of B. okinawaensis differentiate into hermaphrodites and males. The team suggests that the sex of B. okinawaensis nematodes is primarily determined by the stochastic expression of an unknown trigger gene and/or by developmental noise. In other words, sexual differentiation occurs as a result of random events during development.

The team also compared orthologs, ie genes related by common descent, of similar sequences in C. elegans, B. xylophilus and B. okinawaensis. They found that only the downstream genes of these three nematodes were conserved, indicating that the genus Bursaphelenchus has a different sex determination trigger than C. elegans. Additionally, they conducted genetic analyzes and identified a major sex-determining locus in B. okinawaensis, known as Bok-tra-1a. Using bioinformatics and RNA sequencing, they observed conservation of putative targets in this regulatory gene, further confirming findings indicating conservation of downstream functions. This implies that nematode sexual differentiation might have evolved from this downstream regulator.

“Our discovery of a striking new mode of sex determination in the nematode phylum could not only aid laboratory studies of parasitic nematodes, but also contribute to population engineering,” observed Dr. Shinya enthusiastically.

Indicating the importance of these findings in pest control, Dr. Shinya says: “The damage caused by plant-parasitic nematodes is estimated at $80 billion per year. Conventional nematicides are harmful to the environment. Understanding the sex-determining mechanisms of plant-parasitic nematodes can help develop sterile strains that are non-parasitic, but can help reduce nematode populations in a safe and sustainable way. “

Who knew that exploring sex determination in parasitic nematodes would pave the way for disease-free agricultural production and forest protection? We cross fingers !

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Date of publication of the last article May 11, 2022

Research method Experimental study

Subject of research animals

Declaration of conflict of interest The authors declare no conflict of interest

About Associate Professor Ryoji Shinya

Dr. Ryoji Shinya is an associate professor at Meiji University School of Agriculture, Japan. He graduated from Obihiro University of Agriculture and Veterinary Medicine in 2007 and received his Ph.D. from the Graduate School of Agriculture, Kyoto University in 2012. His doctoral work focused on the molecular mechanisms of pine wilt disease caused by the pine nematode Bursaphelenchus xylophilus using genetic approaches , proteomics and phytopathology. As a postdoctoral fellow in the laboratory of Dr. Koichi Hasegawa at Chubu University, Japan, and in the laboratory of Dr. Paul W. Sternberg at Caltech, USA, he studied the biology of C. elegans. He joined Meiji University as a professor in 2017. He is working on establishing a new laboratory model system using B. okinawaensis.