It's somewhat like that when plant-parasitic nematodes (microscopic round worms) play “chemical hide and seek” with their plant host, says plant pathologist Shahid Masood Siddique, an assistant professor in the UC Davis Department of Entomology and Nematology.
“The success of plant-parasitic nematodes depends on their ability to locate a suitable host in the soil,” says Siddique, corresponding author of the newly published Spotlight article, “Chemical Hide and Seek: Nematode's Journey to Its Plant Host,” in the journal Molecular Plant.
Nematodes can be deadly to plants, not only because of the direct damage they cause (they extract water and nutrients from their hosts such as wheat, soybeans, sugar beets, citrus, coconut, corn, peanuts, potato, rice, cotton and bananas) but the role of some species as virus vectors.
“Plant-parasitic nematodes are among the most destructive agricultural pests, causing more than $100 billion in losses per year in the United States,” Siddique said, noting that nematodes are especially damaging to potato, soybean and wheat crops.
Although the success of nematodes depends on their ability to locate a suitable host in the soil, what attracts them to their host “has largely remained unknown,” wrote the four-member UC Davis team of Siddique, Natalie Hamada, Henok Zemene Yimer and Valerie Williams. “Recent studies have revealed that host-seeking by nematodes is a complex process that involves multiple stages in the interaction.”
“Most damage is caused by a small group of root-infecting sedentary endoparasitic nematodes including cyst nematodes and root-knot nematodes (RKNs),” the team of UC Davis researchers wrote in their abstract. “Second stage juveniles (J2s) of plant-parasitic nematodes hatch from eggs into the soil and localize to the roots of host plants. The success of these non-feeding J2s depends on their ability to locate and infect a suitable host.”
For eight decades, scientists have researched the attraction of plant-parasitic nematodes to the host root, ever since the pioneering Maurice Blood Linford (1901-1960) of the University of Illinois, Urbana, Ill., observed in 1939 that the larvae of root-knot nematodes congregate in the cell elongation region behind the root cap.
“Both volatile and soluble components in the rhizosphere have been shown to influence nematode movement,” the UC Davis researchers wrote. “Methyl salicylate, a volatile chemical root signal, has been demonstrated to be a strong root attractant for RKN towards several Solanaceous plants (nightshade family). The non-volatile tomato root exudate quercetin was shown to elicit concentration dependent attraction or repulsion effect against Meloidogyne incognita to host root. Three recent studies have revealed that the recognition of and response to hosts by infective juveniles is a complex process that involves multiple stages in the interaction.”
Siddique focuses his research on basic as well as applied aspects of interaction between parasitic nematodes and their host plants. “The long-term object of our research is not only to enhance our understanding of molecular aspects of plant–nematode interaction but also to use this knowledge to provide new resources for reducing the impact of nematodes on crop plants in California.”
Parents often try to predict the gender of their offspring, but is it possible to predict the sex of a cyst or sexually dimorphic nematode?
Yes, says plant nematologist Shahid Masood Siddique of the UC Davis Department of Entomology and Nematology, who helped develop and validate a strategy to predict the sex of cyst nematodes (round worms) in roots of a mustard family plant in the early stages of infestation.
The research paper, "Host Factors Influence the Sex of Nematodes Parasitizing Roots of Arabidopsis thaliana," published in a recent edition of the journal Plant, Cell and Environment, zeroes in on nematodes parasitizing a small flowering plant widely used in plant biology and known as "mouse-ear cress." Arabidopsis is a member of the mustard (Brassicaceae) family, which includes cabbage and radish. A native of Eurasia and Africa, mouse-ear cress is found throughout much of the United States and Canada.
"We identified the host genes and factors that influence environmental sexual determination of plant parasitic nematodes," said Siddique, the senior author of the paper and an assistant professor at UC Davis. He played a key role in designing and performing the research well as the written work.
The seven-member team, led by Florian Grundler of the University of Bonn, Germany, found that the nematodes that developed at the fastest rate during the first four to 5 days became females, "whereas those that grew slower became mainly males."
"Interestingly, a study by Müller et al. (1981) on comparative food consumption by male and female juveniles from roots of Brassica napus found that females consume about 29 times more food than males," the researchers wrote. "Based on our data and previous literature, we concluded that the difference in food consumption leads to the difference in body volume between the sexes."
The team also included scientists from Germany, Poland, and Pakistan. A DAAD grant from Germany funded the research.
"Plant-parasitic cyst nematodes induce hypermetabolic syncytial nurse cells in the roots of their host plants. Syncytia are their only food source. Cyst nematodes are sexually dimorphic, with their differentiation into male or female strongly influenced by host environmental conditions. Under favourable conditions with plenty of nutrients, more females develop, whereas mainly male nematodes develop under adverse conditions such as in resistant plants. Here, we developed and validated a method to predict the sex of beet cyst nematode (Heterodera schachtii) during the early stages of its parasitism in the host plant Arabidopsis thaliana. We collected root segments containing male-associated syncytia (MAS) or female-associated syncytia (FAS), isolated syncytial cells by laser microdissection, and performed a comparative transcriptome analysis. Genes belonging to categories of defence, nutrient deficiency, and nutrient starvation were over-represented in MAS as compared with FAS. Conversely, gene categories related to metabolism, modification, and biosynthesis of cell walls were over-represented in FAS. We used β-glucuronidase analysis, qRT-PCR, and loss-of-function mutants to characterize FAS- and MAS-specific candidate genes. Our results demonstrate that various plant-based factors, including immune response, nutrient availability, and structural modifications, influence the sexual fate of the cyst nematodes."
Siddique, who joined the UC Davis faculty in March, focuses his research on basic as well as applied aspects of interaction between parasitic nematodes and their host plants. "The long-term object of our research is not only to enhance our understanding of molecular aspects of plant–nematode interaction but also to use this knowledge to provide new resources for reducing the impact of nematodes on crop plants in California."
Plant-parasitic nematodes are microscopic worms that extract water and nutrients from such host plants as wheat, soybeans, sugar beets and bananas. “They're one of the most destructive agricultural pests,” Siddique says. “The agricultural losses due to plant-parasitic nematodes reach an estimated $80 billion. The high impact of plant parasitic nematodes in economically important crops is not only due to the direct damage but also because of the role of some species as virus vectors.”
Shahid Masood Siddique has never met a plant parasitic nematode he didn't like--to study, that is.
Plant-parasitic nematodes are microscopic worms that extract water and nutrients from such host plants as wheat, soybeans, sugar beets and bananas.
“They're one of the most destructive agricultural pests,” says Siddique, an assistant professor with the UC Davis Department of Entomology and Nematology. “The agricultural losses due to plant-parasitic nematodes reach an estimated $80 billion. The high impact of plant parasitic nematodes in economically important crops is not only due to the direct damage but also because of the role of some species as virus vectors.”
“In fact, a recent expert-based assessment of crop health lists nematodes among the most damaging pests and pathogens in different crops. In particular for soybeans, nematodes are the most damaging pests in the United States and around the world.”
Siddique, who joined the UC Davis faculty in March after serving as a research group leader for several years at the University of Bonn, Germany, says nematodes are troubling in other ways as well. “Although nematode-resistance varieties are available for various crops, there is an emergence of resistant-breaking population throughout the world. An example is the recent arrival of peach root-knot nematode in California, which has the potential to seriously harm many of region's important crops including almonds, peaches, eggplants, sugar beets and cucumber.”
Siddique was among a team of scientists from Bonn University and University of Missouri, who demonstrated the ability of parasitic nematodes to synthesize and secrete a functional plant hormone to manipulate the host system and establish a long-term parasitic interaction. PNAS published the research in August 2015. In a subsequent article headlined “Researchers Discover Key Link in Understanding Billion-Dollar Pests in Agriculture,” Science Daily called nematodes “a huge threat to agriculture, causing billions in crop losses every year …The discovery will help to develop crop plants that feature enhanced protection against this type of parasites.”
Born and reared in Multan, Pakistan, Siddique received two degrees in Multan: his bachelor of science degree from the Government College Bosan Road in 2001 and his master's degree in botany from the Bahauddin Zakariya University in 2004. Then it was off to Vienna, Austria to receive his doctorate in 2009 in agriculture and biotechnology from the University of Natural Resources and Life Sciences.
What sparked his interest in nematology? While studying for his masters, he developed a keen interest in molecular biology and biotechnology. For his doctorate, he sought a lab where “I could do my PhD and learn more about cell and molecular biology.” He found that opportunity with Florian Grundler, a professor at the University of Natural Resources and Life Sciences (BOKU), Vienna, Austria.
“His group was working on understanding the molecular aspects of plant-nematode interaction,” Siddique recalled. “In particular, they were using microarrays to study the changes in gene expression in plants upon nematode infection. I found the work very interesting and joined his lab.”
Nematodes did not immediately trigger his interest. “They have a complicated life cycle and infection pattern,” he points out. “Also, it is not yet possible to genetically transform plant-parasitic nematodes. So, I was mostly focusing on plants, which are more amenable to genetic manipulations. Then I gradually started to realize that how fascinating it is to work with nematodes, how they have mastered the ability to manipulate the defense and developmental pathways of their host.”
By the time he completed his doctorate, “I was completely infected by nematodes.” He still is.
What drew him to UC Davis? “High academic reputation in field of agriculture was the main factor that drew me to UC Davis,” Siddique says. “Ethnic diversity and liberal culture of golden state are some of the other factors that contributed to my decision to move to UC Davis.”
“For the next six months, I will be focusing on establishing a state-of-the art nematology lab here at UC Davis. This includes buying equipment, hiring the staff, establishing the protocol, and multiplying the nematode culture. In terms of research, my mid-term goal is understanding the plant immune responses to nematode infections. In long-term, I would like to use this knowledge to produce durable and broad-spectrum resistance in crops.”
“Another area where I will be focusing is development of molecular diagnostic tools for plant-parasitic nematodes from soil,” Siddique says. “I will be particularly focusing on nematodes that are relevant to California agriculture. Lastly, I am highly interested in understanding the mechanism of biocontrol of plant-parasitic nematodes. I expect that this will help in understanding why application of microbial biocontrol is so inconsistent.”
Siddique describes himself as “a result-oriented person and I am comfortable leading a large research team. At the same time, I like to delegate the responsibilities. My working style is collaborative and I believe on open and frank communication.”
In his leisure time, he enjoys cooking, outdoor adventures and watching documentaries. What would people be surprised to know about him? “I am an introvert,” he says. “A couple of other things: I like super spicy food and my favorite game is cricket. And oh, yes, I don't like ice-cold water.”
Siddique is currently seeking “undergraduate and graduate students to work on a number of exciting projects.”
“California is a beautiful place to live,” Siddique says, “and Davis is a perfect place to work on nematodes. So, for those interested in working with nematodes, drop me an email at firstname.lastname@example.org.”
- “Worm Subverts Plant Attack,” The Scientist, April 3, 2014
- “Researchers Discover Key Link in Understanding Billion-Dollar Pests in Agriculture,” Science Daily, Sept. 29, 2015
- “Arabidopsis Leucine-Rich Repeat Receptor–Like Kinase NILR1 Is Required for Induction of Innate Immunity to Parasitic Nematodes,” PLOS Pathogens, April 13, 2017