QnAs with Sheng Yang He

Sheng Yang He has spent a distinguished career studying bacterial plant pathogens and the molecular mechanisms by which they lead to disease. A professor of plant biology at Michigan State University and a Howard Hughes Medical Institute investigator, He was elected to the National Academy of Sciences in 2015. He has used bacterial pathogens, such as Pseudomonas syringae and the virulence factors they secrete, to probe plant–pathogen interactions in the model plant Arabidopsis thaliana. These studies have greatly enhanced our understanding of bacterial pathogenesis, plant immune responses, and the basis of plant disease susceptibility. In his Inaugural Article (1), He provides an overview of recent advances in our molecular understanding of pathogens and insects associated with plant phloem.

Sheng Yang He. Image courtesy of Sheng Yang He.

PNAS: How did you become interested in the interactions between phloem and insects or pathogens?

He: After graduate school, I started my own research project using a fairly simple model system, Arabidopsis and Pseudomonas syringae, and worked with this model for the next 20 years or so. A few years ago, I became interested in studying phloem insects and pathogens. These are some of the most important insects and pathogens in the plant world and are notoriously difficult to study. I had a personal connection to [these types] of insects and pathogens. I grew up in a village in China that grew rice and cotton, and was close to places that grew citrus. So I was quite familiar with the brown planthopper, which is [an] important rice pest globally, and also with citrus greening, a major citrus disease caused by a bacterial phloem pathogen. When I recently visited my undergraduate university in China, Zhejiang University, I talked to my old classmate, Professor Chuanxi Zhang, as well as other colleagues, and we decided to initiate a new collaborative project on phloem-feeding insects and pathogens. Yanjuan Jiang, the Inaugural Article’s (1) first author, is a visiting associate professor who is spearheading this new research direction in my laboratory.

PNAS: What is known about how phloem defends against pathogens and insects?

He: Bacteria and fungi cause disease mainly by secreting virulence “effector” proteins and other molecules into the plant cell that disrupt immune pathways. As for phloem-feeding insects, they use a mouthpiece called a stylet to pierce into the phloem, like a microscopic syringe. Once they reach the phloem, these insects behave like bacteria or fungi in that they inject virulence proteins and likely other molecules into the phloem cell, presumably to shut down the immune response and perturb other host cellular processes. I think one of the immediate things the plant wants to do is probably to isolate the invading pathogen or effector proteins delivered from pathogens and insects. Phloem cells are complex, consisting of specialized sieve cells that form a continuous tube inside the plant for transporting photosynthate, and companion cells next to sieve cells. There are a lot of connections between sieve cells and companion cells, through pores that molecules and probably also pathogens can pass through. These specialized pores can be plugged by polysaccharides called callose, or through proteins that form aggregates. During insect feeding, one of the first things you see is callose deposition that can block these pores. So plugging phloem cell pores could be quite important in phloem defense. Of course, there are other defense responses, which will need to be discovered and characterized.

PNAS: What technical advances are necessary to better understand phloem–pathogen biology?

He: A major barrier to rapid progress in this area is that many of the phloem pathogens cannot be cultured yet. So I think one of the critical areas is to figure out how to grow these pathogens. Other technical advances could include development of phloem cell-specific biosensors to find out what’s really going on in live phloem cells during pathogen and insect attacks in situ, and phloem cell cultures as a tool for studying some aspects of phloem interactions with insects and pathogens. Finally, single-cell sequencing could tell us how the whole transcriptome of phloem cells changes during infection.

PNAS: What future directions are you working on?

He: My laboratory’s main research efforts have been devoted to studying the fascinating plant–pathogen/microbiome interactions and how environmental conditions influence them. For the new phloem–insect–pathogen project in my laboratory, we’re working on two things. One is to attempt synthetic genomics to culture phloem bacteria, and potentially allow any other kind of unculturable bacteria to grow in the laboratory. Another project is to find the host targets of brown planthopper effectors in rice and edit them using CRISPR-Cas9. Our collaborators in Professor Chuanxi Zhang’s laboratory have identified several key effectors of brown planthoppers from insect saliva. We hope to identify the host targets of these insect effectors in rice and edit the corresponding rice genes so they become insensitive to brown planthoppers.

PNAS: What are some of the potential applications of better understanding phloem interactions with insects and pathogens?

He: One of the motivations for this Inaugural Article (1) is to highlight the importance of studying phloem-feeding insects and pathogens. If we can find the vulnerable spots in phloem cells that are attacked by insects and pathogens, we could fix them either chemically or genetically. Can you imagine if we could stop citrus greening, which is devastating the huge citrus industry in Florida and is now in California? And if you could cure brown planthopper in rice, that could transform rice production and result in global increase in the rice yield without indispensable sprays of harmful insecticide. Pathogens and insects are also very useful probes of the fundamental biology of host cells, because they tend to target proteins, RNA, and DNA that are very crucial for host functions. So, I think phloem-feeding insects and pathogens could be really good probes of fundamental phloem biology, and I bet this aspect is also going to be quite interesting to look at in the coming decade.