QnAs with Le Kang

Throughout human history, locusts have remained one of the most destructive insect species in agricultural production. While solitary locusts cause few problems, swarms can destroy billions of dollars’ worth of crops each year and harm the livelihoods of entire communities within days. Institutions such as the United Nations’ Food and Agriculture Organization and the World Bank monitor locust swarms to control plagues. Locust swarms are triggered when the insects undergo a phase transition from the solitary to gregarious states. For the past three decades, Chinese Academy of Sciences zoologist Le Kang has been investigating the ecology and genomes of locusts with an emphasis on the molecular mechanisms of phase transitions. His work has helped solve mysteries in locust plague outbreaks and develop strategies for pest management. Kang was elected as an international member of the National Academy of Sciences in 2021. Kang recently spoke to PNAS about his current research.

Le Kang. Image credit: Jingli Li (Chinese Academies of Science, Beijing, China).

PNAS: How did you become interested in studying phase transitions in locusts?

Kang: Locust phase transition is a fascinating and important biological phenomenon in entomology. I have been captivated by this topic since my undergraduate years. Later, as a laboratory teacher, I collected a large number of locust specimens from the fields for experimental material and observed many differences between gregarious and solitary locusts as well as variations between different geographic populations. These two scientific questions have remained with me throughout my graduate training and long-term academic career. Since 2000, I have been using gene expression and regulation to reveal the mechanisms of phase transition in locusts, which differed from the previous study paradigm focused on behavior, physiology, and endocrine regulation.

PNAS: Your Inaugural Article (IA) examines the changes in RNA translation machinery that occur when locusts transition from the solitary to the gregarious phase (1). Why are locust phase transitions important?

Kang: Locusts display a phase transition in response to changes in population density. It’s a phenomenon called phenotypic plasticity, or polyphenism, and involves remarkable phenotypic variation without a change of genotype. When a group of four or five solitary locusts gather, they release 4-vinylanisole, an aggregation pheromone, that attracts more locusts. Eventually, this attraction causes a transition from the solitary to the gregarious phase.

Solitary locusts do not cause severe economic loss while scattered. On the other hand, gregarious locusts form high-density hopper bands and migratory swarms that result in devastating natural and agricultural disasters worldwide. This transition triggers the outbreaks of locust plagues.

Chemical pesticides are often applied to reduce locust density and suppress the occurrence of plagues. However, the widespread use of chemical pesticides inevitably brings ecological, environmental, and health problems. Cracking the mystery of phase transitions in locusts is an essential step in understanding polyphenism and developing sustainable and environment-friendly control approaches for locust plagues.

PNAS: What did you uncover about locust phase transitions in your IA?

Kang: Although there are many phenotypic differences between the two locust phases, the variations do not involve genetic changes. The strategy of adapting to the environment by altering ribosomal components is common in the biological world. So we suspected that translational regulation could be involved in locust phase transition.

We initiated an investigation into translation regulation under differing population densities. It turns out that locusts do employ distinct translation strategies to reprogram protein synthesis in response to changes of population density. In gregarious locusts, genes encoding cytosolic ribosome subunits had higher translation efficiency, whereas genes encoding mitochondrial ribosome subunits had higher efficiency in solitary locusts. Deletion of two cytosolic ribosome genes and one mitochondrial ribosome gene led to shifts in phase-related behaviors.

At the translational level, we demonstrated that the large ribosomal protein 7 (RPL7) and mitochondrial small ribosomal protein 18c (MRPS18c) affected the ribosomal profiles and behavioral changes in solitary and gregarious locusts, respectively. Crowded ribosomes in gregarious locusts meet the increased protein demand required to support their highly migratory and aggressive lifestyles. This research uncovers the translational regulation of locust behavior, extending the understanding of locust phase transition, and it provides insights into the phenotypic plasticity of locusts.

Furthermore, our findings revealed the crucial role played by dopamine, a neurotransmitter, and its synthesis genes—henna and pale—in the locust phase transition through transcriptional regulation. We identified microRNAs that target the two genes and downstream pathways that regulate the phase changes. Although pale mRNA did not exhibit significant differential expression between the gregarious and solitary locusts, we observed that it had higher expression at the protein level in gregarious locusts. These studies have advanced understanding of phase changes in locusts from transcriptional and posttranscriptional to translational levels.

PNAS: What are the implications of this research? How might it aid in our ability to prevent locust infestations?

Kang: Phase change in locusts is a surprising example of phenotypic plasticity that involves multiple levels of regulation, from olfactory senses to behavior, and from transcriptional, posttranscriptional, epigenetic to translational regulation.

The Inaugural Article reported that locusts can quickly coordinate the efficiency of two different translation systems, cytoplasmic and mitochondrial, to respond to changes in population densities, resulting in reversible behavioral transitions. Our data suggest that translational regulation is a rapid and effective mechanism for locusts [to respond] to environmental cues. In the future, new data at single-cell resolution or derived from specific tissues will help to elucidate the accuracy of translation regulation in locusts.

The proteins and enzymes involved in locust phase transition are ideal targets. If we can identify the key proteins that trigger the phase change, we could develop innovative pesticides to stop this process and prevent costly plague outbreaks.

PNAS: How does the IA fit into the broad themes of your research? Where would you like to take this research in the future?

Kang: Our research has been dedicated to uncovering the molecular regulatory mechanisms underlying locust phase changes across multiple domains, including behavior, body coloration, metabolism, immunity, aging, and reproduction.

Many animals can adjust their survival strategy in response to population density changes using intrinsic regulators. However, unlike mitochondrial–cytosolic translational balance mechanisms in worms, humans, and mice, gregarious and solitary locusts employ a divergence of translational profiles. Disrupting translational balance through mutations in mitochondrial ribosomal proteins can lead to severe neurological defects, depletion in heart and skeletal muscle, and cardiovascular disorders. Further studies are needed to elucidate the metabolic plasticity at the translational level in mitochondria-rich muscle tissues in locusts.

Understanding mechanisms of impaired energy conversion in locusts may provide insights into human diseases, including mitochondrial, neurodegenerative, cardiovascular, and metabolic diseases. In the next 5 to 10 years, we will be working to develop locust models to study human diseases, especially Parkinson’s disease, depression, and other disorders. Our group has [developed] genetic manipulation techniques that will facilitate these efforts.

To better understand locust self-regulation in response to changes in population density as well as its benefits for the insects themselves and their offspring, we want to identify upstream regulatory factors. The rapid development of ribosome profiling technologies will enable in-depth revelation of translational dynamics in phenotypic plasticity.