The people behind the papers: Jun-Ho Ha, Hyo-Jun Lee and Chung-Mo Park

Our 20th instalment of this series comes from South Korea and features an investigation into the molecular basis of how temperature influences developmental transitions in Arabidopsis seedlings, recently published in Developmental Cell. We caught up with joint first authors Jun-Ho Ha and Hyo-Jun Lee, and their supervisor Chung-Mo Park, Professor in the Department of Chemistry, Seoul National University (SNU), to hear the story of the paper.

Chung-Mo, can you give us your scientific biography – I understand you spent some years in the US before returning to South Korea?

CMP I am currently professor in the Department of Chemistry at SNU. I earned my Bachelor of Science in the Department of Science Education from Seoul National University in 1983 and my PhD in molecular virology from State University of New York at Buffalo in 1993 under the supervision of professor Jeremy Bruenn. The topic of my thesis work was identification of killer toxin genes in a double-stranded virus endogenously residing in Ustilago maydis, a corn smut fungus and functional and structural characterization of the killer toxin proteins. After completing my PhD, I worked as a postdoctoral researcher in the same university and the Hauptman-Woodward Medical Research Institute, Buffalo, until I joined the Kumho Life & Environmental Science Laboratory, Korea, as PI in 1996. In the Kumho Laboratory, I worked on the photochemical and photobiological characterization of phytochrome photoreceptors in higher plants and the cyanobacteria Synechocystis PCC6803 and their associated light signal transduction in photomorphogenic responses.

In 2002, I accepted an associate professor position in the Department of Chemistry, SNU, where I have been since that time. While at SNU, my research team has been working on diverse aspects of plant growth and developmental processes, such as seed germination, phase transition and flowering induction, and leaf senescence. I have also been working on plant responses to environmental stresses with emphasis on temperature extremes and drought stresses. In recent years, my research is focused on plant adaptation to high but nonstressful temperatures (warm temperatures) with emphasis on leaf hyponasty, heat dissipation from leaves, and autotrophic development.

And what is South Korea like as a place to do science?

CMP The Korean government and several biotech companies have been investing a huge amount of research fund during the last 30 years. While industrial research and development has been a priority as a potential driving force of economic growth, the Korean government is also spending heavily on basic research. In plant science, there is a national research supporting program, termed New-Generation Biogreen 21, which is organized and supported by the Korean Rural Development Administration.  The Program supports various research on both model plants and crops. It is considered that although not sufficient, enthusiastic plant scientists are able to get enough research funds to perform both basic and applied researches in recent years.

Jun-Ho and Hyo-Jun – how did you come to join Chung-Mo’s lab?

JHH I earned my Bachelor of Science in chemistry. I was also interested in molecular biology with an expectation that combining chemical and biological principles would be exciting in understanding life. While I was looking for an appropriate lab for my graduate study, I met Chung-Mo Park, who is my current thesis advisor. I was greatly impressed by his passion for science and research. It was also impressive that his group is working on plant molecular biology in the Department of Chemistry. I therefore decided to join his laboratory for my graduate study.

HJL Since I was a high school student, I planned to be a scientist with an aim of discovering unknown principles of nature and living organisms. After I entered the Department of Chemistry, Seoul National University, as an undergraduate student, I searched for potential labs in the Department appropriate for my research carrier. I realized that Chung-Mo’ lab is unique among the laboratories in that he is studying plant molecular biology and biochemistry. I thought that understanding molecular biological and biochemical mechanisms underlying plant performance would be helpful for me to find ways to sustain the Earth’s ecosystem. In particular, as a chemist, I thought that applying chemical tools to understanding biological systems would be interesting. I therefore decided to perform my graduate study in his lab.

Before your work, what was known about how plants respond to temperature changes during autotrophic development, and what was the key question you set out to answer?

CMP, JHH & HJL It is well known that extreme temperatures significantly affect plant performance, including autotrophic development. In addition, associated molecular events and signaling schemes are fairly well understood. In nature, the soil temperature is rapidly elevated under warm temperature conditions. Therefore, developing seedlings should cope with high temperatures while they pass through the heat-absorbing soil layer to obtain photosynthetic capacity required for autotrophic growth. However, it is almost unknown how the heat-labile shoot apical meristem tissues of developing seedlings handle the temperature constraints. It has recently been reported that warm temperatures, in a temperature range of 23 – 28^oC in Arabidopsis, accelerate cell elongation during early seedling development. Thus, we were curious about whether and how warm temperatures influence chlorophyll biosynthesis during autotrophic development.

Can you give us key results of the paper in a paragraph?

CMP, JHH & HJL We demonstrated that developing seedlings are capable of maintaining chlorophyll biosynthesis required for autotrophic development at warm temperature conditions. A group of photooxidoreductase (POR) enzymes is responsible for chlorophyll biosynthesis. Notably, they are susceptible to warm temperatures and thus rapidly inactivated in developing seedlings while they pass through the warm soil layer. We found that an RNA-binding protein FCA maintains the abundance of POR enzymes at warm temperatures in developing seedlings. Without FCA, plants fail to maintain the enzyme abundance, resulting in loss of chlorophyll and thus failure to achieve autotrophic growth. Our work provide a molecular basis for the acquisition of autotrophic growth under fluctuating temperature conditions in plants.

How do have any idea of what is upstream of FCA? How does it sense temperature changes?

CMP, JHH & HJL Our recent findings strongly support that the typical RNA-binding protein FCA plays a critical role through epigenetic control of target genes during high temperature responses and thermomorphogenesis in Arabidopsis. Our data also indicate that FCA sustains the thermos-stable expression of POR enzymes during autotrophic development at warm temperatures. Altogether, these observations suggest that FCA function is thermos-regulated. However, it is current unclear how FCA is activated by ambient temperatures. We found that gene transcription and protein stability of FCA are not altered by temperature changes. Its subcellular localization is also unaltered under fluctuating temperature conditions.

Our preliminary data suggest that warm temperatures activates FCA through post-translational modifications, such as protein phosphorylation. We are currently under way to examine if FCA is differentially phosphorylated or chemically modified in response to temperature changes by employing global-scale proteomics.

Do you think your work will have relevance to agriculture in a warming world?

CMP, JHH & HJL Global warming depicts the gradual elevation of the average temperature of the Earth’s climate system. It is widely documented that under high ambient temperature conditions, plants exhibit distinct morphological and developmental traits, such as accelerated hypocotyl growth, leaf hyponasty, reduction of stomatal density, and early flowering, which profoundly influence crop productivity and commercial values. Our findings on plant thermal responses are closely associated with global warming. We propose that the FCA-mediated thermal adaptation of autotrophic development allows developing seedlings to cope with the heat-absorbing soil surface layer under natural conditions. In particular, we found that a single gene mutation causes a total loss of chlorophyll biosynthesis and autotrophic development at warm temperatures, providing a way of enhancing plant adaptation to thermal fluctuations in crop agriculture.

When doing the research, did you have any particular result or eureka moment that has stuck with you?

HJL & JHH In the initial stage of the research, we germinated and grew the FCA-defective mutants at normal temperatures for 3 days before transferred to warm temperatures to see if the fca mutations affect seedling growth. However, we did not observe any phenotypic differences in seedling growth and greening patterns in the mutants. A few months later, we anticipated that the fca mutations might affect the earlier stages of seedling growth. To examine the hypothesis, we germinated and grew the mutant seedlings at 28^oC. We were surprised at the albino phenotype of the mutants. This observation triggered the re-examination of the thermal phenotypes of the fca mutants, resulting in the completion of this paper.

At first, we could not figure out why the fca mutants exhibited albinism only when germinated and grown at warm temperatures. As a potential cause of the albino phenotype, we considered several possibilities, such as defects in chloroplast development, chlorophyll biosynthesis, or both. It was found that the expression of POR genes was disrupted in the fca mutants when grown at warm temperatures. Accordingly, the level of chlorophylls was extremely low in the mutants, showing that the thermo-sensitive albino phenotype of the mutants is caused primarily by defects in chlorophyll biosynthesis, consistent with the FCA-mediated stabilization of POR production.

And what about the flipside: any moments of frustration or despair?

HJL & JHH The FCA-defective mutants are well-known late flowering mutants. A set of transgenic fca plants expressing POR genes were required for this study. It needs a lot of time to generate the transgenic plants because it takes 3-4 months to obtain seeds from the transgenic plants. While we were generating transgenic plants, we realized that a wrong expression construct was accidentally used, spending at least 5 additional months to obtain correct transgenic plants.

We also remember the frustrating moment when temperature controllers in the culture room were out of order during last summer, when we experienced a rarely high temperature and thus unstable supply of electricity in Korea. We had to grow a full set of plants again after a period time for fixing the temperature controllers.

What are your career plans following this work?

HJL I am currently a postdoc in Chung-Mo Park’s lab. I will continue studying for a while on molecular and physiological mechanisms underlying plant thermomorphogenesis. I am interested in the as-yet unidentified regulator of POR abundance at warm temperatures. After finishing the experiments, I am planning to find an appropriate postdoc position to extend my research career in environmental control of plant proteomics.

JHH I hope to be able to finish my thesis study in a couple of years, after which I am planning to find postdoc positions in Korea or in USA to extend my research career in the field.

And what next for the Park lab?

CMP We have a well-organized research system with a variety of molecular and biochemical tools, personnel, and facilities. We are specialized in gene regulatory mechanisms with emphasis on induction and activation mechanisms of transcription factors. Using these research tools and system, we will further extend our researches on plant thermomorphogenesis, which is emerging as a hot issue in the field because of the growing concern about global warming. In particular, we are focused on the functional linkage between photomorphogenic responses and growth hormones. We are also preparing a long-term project for engineering crop plants to enhance their adaptation capacity to changing temperature environment.

Jun-Ho Ha, Hyo-Jun Lee, Jae-Hoon Jung and Chung-Mo Park. 2017. Thermo-Induced Maintenance of Photo-oxidoreductases Underlies Plant Autotrophic Development. Developmental Cell 41(2): 170-179.

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