Plants respond to changes in temperature using complex mechanisms, with decreases in temperature inducing vernalisation and high temperatures causing thermo-morphogenesis. A new paper in Development investigates how VIL1, a PHD finger-containing protein, functions in plants during thermo-morphogenesis. To find out more about this research, we spoke with co-first author of the study, Junghyun Kim, and corresponding author Sibum Sung (Associate Professor of Molecular Bioscience at the University of Texas in Austin, USA). Co-first author Yogendra Bordiya was not available to interview, having now moved to a different sector.

Sibum Sung (L) and Junghyun Kim (R)

Sibum, can you give us your scientific biography and the questions your lab is trying to answer?

SS: My research focus has been to understand the mechanistic details of epigenetic regulation of plant development, including the vernalization response of plants, a classical model of epigenetic regulation by environmental changes. My group aims to clarify how environmental cues (such as temperature and light) can influence epigenetic regulation of developmental programs in eukaryotes. Notably, we want to reveal mechanistic details of the roles of genome structure changes in environmentally induced development reprogramming.

Junghyun, how did you come to work in Sibum's lab and what drives your research today?

JK: During my Ph.D. training, I studied how light sensors, together with their interacting key transcription factors, trigger transcriptional regulation to control downstream morphological changes in response to environmental changes. My research focus was on the in vivo DNA binding specificity of those transcription factors, but I also realized that understanding epigenetic regulation is essential to fully describe mechanistic details of gene regulation by the environment in eukaryotes. Dr Sung's group studies mechanisms underlying epigenetic regulation of plant development by environmental changes, such as temperature and light. Thus, it was a perfect fit for my postdoctoral position.

What was known about thermo-morphogenesis before your work?

SS & JK: A lot was known, and there is much more to learn! Over the last several years, it has been fascinating to witness several breakthroughs in our understanding of mechanisms underlying thermo-morphogenesis in plants. Multiple signalling pathways and regulatory modules at the level of gene expression have been identified. There are multiple routes through which plants perceive and translate warm temperature into their developmental reprogramming. For example, the phytochrome B-PIF4 regulatory module and the eviction of a histone variant, H2A.Z, have been extensively studied. However, it is clear that there could be more mechanisms because, essentially, all plant physiology would be affected by temperature.

A lot was known, and there is much more to learn! Over the last several years, it has been fascinating to witness several breakthroughs in our understanding of mechanisms underlying thermo-morphogenesis in plants

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

SS & JK: This work was initiated by an unexpected observation that vil1 mutants exhibit hyposensitivity to high ambient temperature. Given that VIL1 is a facultative component of the H3K27 methyltransferase complex, PRC2, we interrogated how the loss of VIL1 affects thermo-morphogenesis. It turned out that genome-wide H3K27me3 accumulation occurs when plants are grown in warm temperatures, and the increase in H3K27me3 requires VIL1.

How do you propose VIL1 regulates H3K27me3?

SS & JK: Previous studies have shown that VIL1, as a PHD-finger-containing protein, is a facultative component of PRC2, which mediates H3K27me3. Unfortunately, we still don't know how VIL1 can enhance the PRC2 activity and thus H3K27 methylation. We have several working models to test, so stay tuned!

Were you surprised to find that arp6 mutant phenotypes can be rescued by the loss of VIL1?

JK: Yes, definitely. arp6 mutants show a number of developmental anomalies, but most phenotypes of arp6 mutants were suppressed in the arp6 vil1 double mutants. It was also striking when we observed that vil1 mutations also restored transcriptome changes of arp6 to the wild-type level in arp6 vil1 mutants.

Flowering phenotype of Col-0, vil1-1, vil1-2 and VIL1-myc/vil1-1 plants grown at continuous 22°C or 27°C in short-day conditions. Each photo was taken at 13 weeks (22°C) or 7 weeks (27°C) after germination.

Flowering phenotype of Col-0, vil1-1, vil1-2 and VIL1-myc/vil1-1 plants grown at continuous 22°C or 27°C in short-day conditions. Each photo was taken at 13 weeks (22°C) or 7 weeks (27°C) after germination.

What implications will your study have for understanding the effects of climate change on plant development?

SS & JK: As we discussed earlier, multiple layers of regulatory modules exist in plants to deal with temperature changes. Our work added another important regulator, Polycomb-mediated histone modification, into the mix. Climate change inevitably affects biodiversity and crop yield. Understanding thermo-morphogenesis and underlying mechanisms would provide us with tools to cope with the challenges we are facing.

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

JK: When we observed VIL1-dependent genome-wide accumulation of H3K27me3 in high temperatures by ChIP-seq, we thought the H3K27me3 accumulation might be a local effect. However, when we observed significant increases of H3K27me3 using western blot analysis, we realized that the VIL1-dependent H3K27me3 accumulation is one of the crucial events in thermo-morphogenesis.

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

JK: It was exciting to find that VIL1 is necessary for the high temperature-mediated H2A.Z eviction. However, we could not figure out how. We have a few hypotheses to test, but we do not have the answer yet.

Junghyun, what is next for you after this paper?

JK: I am currently working on several other projects related to temperature response in plants, including a follow-up of this work. As a postdoctoral fellow, I am also developing other skills to become an independent researcher in the near future.

Sibum, where will this story take your lab next?

SS: Over the last several years, we uncovered that VIL1, as a facultative component of PRC2, mediates chromatin responses to various environmental stimuli. The question now is how VIL1 modulates PRC2 activity in a stimulus-specific manner, including warm ambient temperature. We have a few working hypotheses to test, which will be the lab's main focus.

Finally, let's move outside the lab – what do you like to do in your spare time?

JK: Most of the time, I hang out with my kids and spend time with my family. I love family camping, travel and biking. I also enjoy baking.

SS: Austin has lots of beautiful trails to hike. When I am not in my office, I sometimes walk around one of those trails.

Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712, USA.

E-mail: [email protected]

Kim
,
J.
,
Bordiya
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Y.
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Xi
,
Y.
,
Zhao
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B.
,
Kim
,
D.-H.
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Pyo
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Y.
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Zong
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W.
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Ricci
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W. A.
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Sung
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S.
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2023
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Warm temperature-triggered developmental reprogramming requires VIL1-mediated, genome-wide H3K27me3 accumulation in Arabidopsis
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