20 years! Cracking the "unique skill" of super pests

Bemisia tabaci, photo courtesy of the Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences

■Reporter Li Chen

"'Using the spear of the son, the shield of attacking the son" is an allusion during the Warring States Period.

This "unique skill" enables Bemisia tabaci to feed on more than 600 kinds of plants and harm global crops.

On March 25, "Cell" published the results of this collaboration between Chinese and foreign scientists online.

The mystery of "food habits"

In 1996, a pest that resembled the whitefly whitefly in a greenhouse was discovered in a vegetable greenhouse in Beijing.

This is the pest Bemisia tabaci that has invaded our country.

"From then on, the mystery of insect feeding habits became a lingering question in my mind.

Some insects only feed on one plant, such as brown planthopper, which only eats rice, which is monophagous; some can eat multiple plants within a family or related families, such as Plutella xylostella only feeds on cruciferous vegetable crops, called widowhood.

Why do insects eat different plants? Polyphagous pests have strong adaptability, how to prevent them? Feeding habits are obviously closely related to the outbreak of pests.

Xia Jixing, the co-first author of the paper, told the Chinese Journal of Science that after insects feed on host plants, they will induce host plants to produce a defensive response and produce a large number of secondary metabolites that are toxic to insects, leading to the death of most insects.

Secondary metabolites are important weapons for plants to resist pests, just like a "shield.

"Bemisia tabaci can eat more than 600 kinds of plants, indicating that it can resist the secondary metabolites of most plants.

Bemisia tabaci not only causes direct damage by sucking the phloem sap of the host plant, but also can secrete honeydew to induce plant fungal diseases such as coal pollution and damage plants.

Since 2001, the team has concentrated on the host adaptability of Bemisia tabaci and the mechanism of its outbreak.

Through the detection of more than 6000 samples from more than 260 field populations across the country, as well as the research on the allele frequency, differentiation coefficient and gene flow among the populations, they clarified the current status of the invasive distribution of Bemisia tabaci in my country and the invasive populations.

"These works laid the foundation for us to analyze the molecular mechanism of Bemisia tabaci to phenol sugar detoxification.
" Zhang Youjun said.

Steal the "spear" of plants

Starting with the secondary metabolites of plants, Zhang Youjun’s team analyzed the metabolic profile of tomato leaves, one of the favorite foods of Bemisia tabaci, and detected 9873 compounds, of which 290 phenol sugars were identified, accounting for 2.
93%.
Phenol sugar is an important class of insect-resistant secondary metabolites of plants, which can inhibit the growth and development of insects.

The amazing thing is that the phenol sugars secreted by the plants themselves are also harmful to the plants themselves.
"Too much phenol sugar is not good for plant growth and development.
" said Guo Zhaojiang, the co-first author of the paper and a researcher at the Vegetable Research Institute.
Therefore, when the pests leave, plants must quickly degrade the excess phenol sugars.

The "antidote" that plants prepare for themselves is phenol sugar malonyl transferase (PMaT).
The malonylation reaction of phenol sugar catalyzed by it plays an important "detoxification" effect in the life process of plants.

So, how does Bemisia tabaci, which like to eat tomato leaves, deal with phenol sugars?

The past chemical analysis can no longer answer this problem.
For a period of time, the research on the detoxification mechanism of Bemisia tabaci has been slow.

In 2009, Q-type Bemisia tabaci broke out in a large area in China and spread the virus on tomatoes, causing economic losses of more than 10 billion yuan.
The prevention and control of Bemisia tabaci is of urgency.

At this time, advances in genome sequencing technology brought hopes of breaking through the bottleneck.
Zhang Youjun's team decided to sequence the genome of the Q-type Bemisia tabaci.
In 2013, the Bemisia tabaci genome was sequenced and 20786 genes were obtained.

Yang Zezhong, the co-first author of the paper, told the China Science Daily that in the process of analyzing the genes related to the complex advanced functions and biological systems of Bemisia tabaci, "we discovered the gene that was later named BtPMaT1.
I felt very excited at the time.
" .

Because they later proved that the Bemisia tabaci gene is homologous to the plant's phenol sugar malonyl transferase.

"The BtPMaT1 gene does exist in the Bemisia tabaci genome, not the plant genome contamination.
" Zhang Youjun said that the phylogenetic tree analysis showed that the homologous gene of the Bemisia tabaci BtPMaT1 gene only exists in plants and a small number of fungi.
"This is the gene'stolen' from the plant by Bemisia tabaci.
This is a horizontal gene transfer phenomenon that is widespread in the biological world.
" Zhang Youjun said.

Previous studies have proven that horizontal gene transfer often occurs between prokaryotes, and is generally considered to be the driving force for the evolution of prokaryotes.
More and more evidences show that horizontal gene transfer is also an important factor in the adaptive evolution of eukaryotes.

However, almost all gene donors for arthropod horizontal gene transfer events are microorganisms, and experimental evidence for horizontal transfer of plant-derived functional genes to insects has been lacking.

The co-corresponding author of the paper, chemical ecologist and entomologist Ted Turlings of the University of Neuchâtel, Switzerland, said: “This study provides the first internationally functional evidence of the horizontal transfer of plant genes to insects, which can metabolize plants.
The gene for defensive toxins, BtPMaT1, only exists in Bemisia tabaci.
"

Through in vitro cell expression enzyme activity analysis, Bemisia tabaci midgut tissue enzyme activity analysis and Bemisia tabaci excreta enzyme activity metabolism analysis, it is found that this gene still performs the same function as the plant homologous gene—detoxifies phenol sugars.

"The'spear' of the plant was stolen by the whitefly, but turned into a'spear' that attacked the plant.
" Zhang Youjun said.

Countermeasures with RNA interference

"We think that a certain virus in plants may carry the BtPMaT1 gene.
After being eaten by the whitefly, the virus integrates the gene into the whitefly's genome through an unknown mechanism.
" Turlings said, "Of course.
, This is a seemingly impossible thing to happen, but imagine that billions of insects, viruses, and plants evolve over time over the course of millions of years.
This happens occasionally, if the acquired genes are harmful to insects.
Favorable, then it will evolve to be more favorable and spread widely.
"

After revealing the molecular mechanism of Bemisia tabaci’s incredible adaptability, Zhang Youjun’s team developed a strategy to crack the “super power” stolen by Bemisia tabaci, that is, using RNA to interfere with the BtPMaT1 gene of Bemisia tabaci to make it right This plant is sensitive to toxic compounds.

RNA interference refers to a phenomenon that is highly conserved in the evolutionary process, induced by double-stranded RNA, and homologous mRNA is efficiently and specifically degraded.
Its role is to silence related genes.

Here, "We made hairpin RNA using fragments of the BtPMaT1 gene, and fed the hairpin RNA directly to Bemisia tabaci.
The interference efficiency was about 50%.
After silencing the gene, three phenol sugar treatments caused the death of Bemisia tabaci.
The rate increased by about 20%.
" Zhang Youjun said.

In addition, they also constructed a genetically modified tomato line expressing the hairpin RNA.
They found that in the excreta of Bemisia tabaci eating genetically modified tomatoes, the content of some phenolic sugars increased, and the acylation products of some phenolic sugars decreased.

"Without the action of pesticides, the mortality rate of Bemisia tabaci was 15.
48% after eating wild tomatoes for 7 days, and the mortality rate of Bemisia tabaci was 93.
35% after eating transgenic tomatoes for 7 days.
However, for non-target arthropods, aphids and spider mites No effect.
" Guo Zhaojiang said that genetically modified tomato strains can effectively control Bemisia tabaci.

"Of course, the application of this method still needs to overcome some obstacles, the most obvious is people's worries about genetically modified crops.
" Turlings said, "but in the future, I do think that this is a green, efficient and safe method for whitefly control.
Because the gene is derived from a plant, and now that we have a clear mechanism of its action, we are also able to deal with possible changes in the Bemisia tabaci gene.
"

"The gene transferred into this genetically modified tomato is a plant homologous gene, so it is more green and efficient.
It may be applied to the whitefly control process in the future.
" Zhang Youjun said that they have applied for a Chinese national invention patent.

Related paper information:

https://doi.
org/10.
1016/j.
cell.
2021.
02.
014