March 5, 2015

Zhang et al. "Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids"

Jiang Zhang, Sher Afzal Khan, Claudia Hasse, Stephanie Ruf, David G. Heckel, Ralph Bock*

Science 27 February 2015:Vol. 347 no. 6225 pp. 991-994 DOI:10.1126/science.1261680

Crop protection in large scale agriculture is a necessity given the many unintended consequences of traditional breeding. One of these consequences was the elimination of many natural plant defenses against insects, which consisted partly of the accumulation of bitter and poisonous secondary metabolites which made them unappealing for insects to eat. In our aeons long quest to make a better tasting tomato, our breeding experiments naturally resulted in food that tasted better to us by eliminating those same bitter, poisonous metabolites. And insects could not thank us more for our efforts, as they find our domesticated plants even tastier than their wild type cousins. A considerable amount of scientific energy has therefore been invested in devising strategies that protect crops intended to fill our pantries from their natural enemies: the rest of nature.

Pesticides of all sorts were synthesized in the last century and applied to crops in order to protect them from insects and other pests of agriculture. And they worked quite well; we still use them in massive amounts. But they have disadvantages too, like the effects of some pesticides on human health and that of other animals. The era of genetic engineering ushered in a new suite of techniques to confront the problem of insects (or better, arthropods) trying to eat our food. The Bt toxin, derived from the soil bacterium Bacillus thuringensis, is an effective strategy for reducing crop losses. The gene encoding this protein can be expressed in the tissues of crops using genetic transformation. To most animals including humans, it's just another protein in the plant among tens of thousands that is digested like the rest. But the Bt protein shows extremely high, specific toxicity towards several important agricultural pests, so plants expressing it rapidly kill of pests with no effects on us. But Bt resistance is sure to emerge in the long run, and may be happening already. Fortunately, scientists are aware of this problem and have concentrated their efforts on ever more efficacious and sustainable approaches to reducing crop losses.

The report by Ralph Bock's group at the Max Planck Institute for Molecular Plant Physiology cited above is a striking example of a major advance in our ability to control insect pests in agriculture using technology. Their approach uses RNAi interference to highjack insects' own self-defense system. For most plants and animals, the presence of double stranded RNA (dsRNA) inside the cell signals an impending viral infection, and the natural, evolved immune response against this type of attack involves an inducible defense system which includes a protein called Dicer. Dicer cleaves the dsRNA into smaller fragments about 21 bp in length called small interfering RNA (siRNA). These fragments are then used to locate and destroy other RNAs in the cell that match it, providing a threat identification system of sorts. Insects have the unusual property that some of the RNA they consume is not degraded right away. Some can even enter the cell and exert biological effects. This ordinarily has little effect on them, but scientists have long considered the possibility of engineering plants to produce dsRNA directed against transcripts critical to insect survival. For various reasons, this approach didn't work very well, party because plants also have a similar RNAi defense system that cleaves the long dsRNAs into smaller pieces before they are attacked by insects, rendering this approach less effective. Zhang et al. took a further step in their expression of insect dsRNAs in plants: they expressed them directly in the plastid, an organelle which has its own genome and translational machinery but no RNAi system. By doing so, they circumvented the plant´s RNAi induction and produced plants which accumulated large amounts of intact, insecticidal dsRNA in plant plastids. When their transgenic (in this case, transplastomic) potato plants were subjected to feeding by the Colorado potato beetle, a devastating pest, the plant dsRNA matching the beetle actin gene induced the RNAi response of beetles against their own genes. In this way, the plants can be effectively protected against a significant pest without the application of chemical pesticides. Since chloroplasts are maternally inherited and not released in pollen, their dissemination in the environment can be controlled. And it immediately creates a barrier to developing resistance since insects would have to mutate a highly conserved gene to overcome RNAi induction against their own genes. In that case, plants can be re-transformed with a new dsRNA sequence to confront any evolved resistance by simply sequencing the genome of resistant pests. Congratulations to Jiang Zhang and co-workers for this interesting application of plastid engineering to provide an environmentally sound solution to a major problem in agriculture.

From the article:


Double-stranded RNAs (dsRNAs) targeted against essential genes can trigger a lethal RNA interference (RNAi) response in insect pests. The application of this concept in plant protection is hampered by the presence of an endogenous plant RNAi pathway that processes dsRNAs into short interfering RNAs. We found that long dsRNAs can be stably produced in chloroplasts, a cellular compartment that appears to lack an RNAi machinery. When expressed from the chloroplast genome, dsRNAs accumulated to as much as 0.4% of the total cellular RNA. Transplastomic potato plants producing dsRNAs targeted against the β-actin gene of the Colorado potato beetle, a notorious agricultural pest, were protected from herbivory and were lethal to its larvae. Thus, chloroplast expression of long dsRNAs can provide crop protection without chemical pesticides.

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