MECHANISMS OF LIGHT AND TEMPERATURE SIGNALING BY PHYTOCHROME B

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 1019378
• Project Start Date: Apr 19, 2019
• Project End Date: Sep 30, 2023
• Program Code: [(N/A)]- (N/A)

Recipient Organization
UNIVERSITY OF CALIFORNIA, RIVERSIDE
(N/A)
RIVERSIDE,CA 92521

Performing Department
Botany and Plant Sciences

Non Technical Summary
Light and temperature are major factors governing the distribution and seasonal behavior of plants. Being sessile, plants are highly responsive to light and temperature differences and can adjust their growth and development accordingly. Increases in global temperature have already had dramatic impacts on plant phenology, distribution, diversity, and are expected to significantly decrease crop productivity. This project will focus on understanding the light and temperature signaling mechanisms by the photoreceptor and ambient temperature sensor phytochrome B. In particular, we will determine how phytochrome B controls plant growth through the regulation of gene expression. The expected outcomes of this project will enhance our understanding of the genetic underpinning of how plants respond to changes of light and temperature in their environment, and thus will facilitate rational breeding for thermo-tolerant crop in diverse light environments.

Animal Health Component

(N/A)

Research Effort Categories

Basic

100%

Applied

(N/A)

Developmental

(N/A)

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
203	2499	1030	90%
201	0430	1080	10%

Knowledge Area
203 - Plant Biological Efficiency and Abiotic Stresses Affecting Plants; 201 - Plant Genome, Genetics, and Genetic Mechanisms;

Subject Of Investigation
0430 - Climate; 2499 - Plant research, general;

Field Of Science
1030 - Cellular biology; 1080 - Genetics;

Keywords

climate change

temperature signaling

light signaling

Goals / Objectives
Light and temperature are major environmental factors governing the distribution and seasonal behavior of plants. Being sessile, plants are highly responsive to light and temperature differences and can adjust their growth and development accordingly. Increases in global temperature have already had dramatic impacts on plant phenology, distribution, diversity, and are expected to significantly decrease crop productivity. Understanding the signaling mechanisms underlying the light and temperature responses is particularly relevant in the context of climate change, as this knowledge will be key to rational breeding for thermo-tolerant crop in diverse light environments. Phytochrome B (PHYB) is an evolutionarily conserved red and far-red photoreceptor and an ambient temperature sensor, which integrates environmental light and temperature signals to control almost all aspects of plant development and growth. PHYB controls the diverse downstream morphological, physiological, and developmental responses through the regulation of hundreds of light- and temperature-responsive genes in the nucleus. However, how photoactivation of PHYB triggers genome-wide transcriptional reprogramming is still not fully understood. The goal of this project is to understand the mechanism of PHYB-mediated light and temperature signaling in gene regulation using Arabidopsis as the model and transfer the knowledge gained into crops such as maize, rice, and tomato. We particularly focus on how light and temperature control developmental and growth traits such as seedling establishment, leaf greening (or the biogenesis of photosynthetically-active chloroplasts), as well as leaf and stem growth. Our central hypothesis is that PHYB reprograms the nuclear genomes through two major mechanisms: (1) regulation of the stability and activity of transcription regulators for plant development and growth, and (2) reorganization of the nuclear architecture, including de novo biogenesis of a photosensory subnuclear domain called the photobody and spatial-repositioning of individual genes. We plan to test this hypothesis and, thereby, elucidate light and temperature signaling mechanisms in plants by pursuing the following objectives:(1) Determine the function of photobodies in PHYB signaling. (2) Determine how PHYB signaling controls the central growth regulators PIF3 and PIF4. (3) Determine the mechanism of gene repositioning by PHYB signaling. The project is timely as it seeks to understand and address local and global challenges of climate change. The expected outcomes of this project will elucidate the signaling mechanism by which ambient temperature changes alter plant development and growth and provide the inner works linking genes to temperature-tuned plant phenotypes (or responses). The knowledge gained from this project will facilitate rational breeding for agronomically beneficial traits to cope with climate change.

Project Methods
We will employ a combination of genetics, cell biology, biochemistry, and genomics approaches to achieve the objectives of this project.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:We have published three research articles in high-impact scientific journals, such as Nature Communications. These publications have been accessed online more than 5,000 times each by scientists around the world in the past year. Also, we have presented our work in national and interactional meetings. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project provides training opportunities to one graduate student and one postdoctoral researcher. How have the results been disseminated to communities of interest?We have published our results in high-impact scientific journals and presented our work at national and international conferences. What do you plan to do during the next reporting period to accomplish the goals?We plan to continue investing the function of the newly identified signaling components in light and temperature signaling, in particular in the regulation of PIF4 stabilization in warm temperatures. We will also investigate the mechanism of transcriptional activation by PIFs. Moreover, we will utilize the newly developed method of fluorescentin situ hybridization to investigate light-regulated gene positioning in Arabidopsis.

Impacts
What was accomplished under these goals? We have made significant progress in all three objectives. First, we reported the temperature-induced photobody dynamics. Second, we have identified two new signaling components in PHYB signaling, REGULATOR OF CHLOROPLAST BIOGENESIS and NUCLEAR-CHLOROPLAST CONTROL OF PEP. Third, we have established a new fluorescent in situ hybridization protocol to study gene positioning in Arabidopsis.

Publications

• Type: Journal Articles Status: Published Year Published: 2019 Citation: Yoo CY, Pasoreck EK, Wang H, Cao J, Blaha GM, Weigel D, Chen M. (2019) Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat Commun 10:2629. doi: 10.1038/s41467-019-10518-0.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Yang EM, Yoo CY, Liu J, Wang H, Cao J, Li F-W, Pryer KM, Sun T, Weigel D, Zhou P*, Chen M*. (2019) NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches. Nat Commun 10:2630. doi: 10.1038/s41467-019-10517-1.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Hahm J, Kim K, Qiu Y, Chen M. (2020) Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. Nat Commun 11:1660. doi: 10.1038/s41467-020-15526-z.
• Type: Book Chapters Status: Published Year Published: 2020 Citation: Yoo CY, Han S, Chen M. (2020) Nucleus-to-plastid phytochrome signalling in controlling chloroplast biogenesis. Annu Plant Rev 3:251-280. doi: 10.1002/9781119312994.apr0615.

Progress 04/19/19 to 09/30/19

Outputs
Target Audience:We disseminated our discoveries through publications and research presentations at national and international research conferences. Our primary audience is the worldwide scientific community. In the report period, we published two research articles and one book chapter. I was invited to present our research in the following conferences and seminars: 1. Plenary Talk, Northwest Developmental Biology Meeting, San Juan Island, WA 2. Plant Biology Department, the Salk Institute, La Jolla, CA 3. International Symposium on Plant Photobiology, Barcelona, Spain 4. 30th International Conference on Arabidopsis Research, Wuhan, China Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project provided training opportunities to one postdoctoral researcher and one graduate student. How have the results been disseminated to communities of interest?In the reporting period, we published two research articles and one book chapter. I was invited to present our research in the following conferences and seminars: 1. Plenary Talk, Northwest Developmental Biology Meeting, San Juan Island, WA 2. Plant Biology Department, the Salk Institute, La Jolla, CA 3. International Symposium on Plant Photobiology, Barcelona, Spain 4. 30th International Conference on Arabidopsis Research, Wuhan, China What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period, we will focus on the following goals: (1) We will define the temperature-dependent photobody dynamics, and(2) Will determine the transcriptional activation mechanisms by the two critical growth-promoting transcription factors, PIF3 and PIF4.

Impacts
What was accomplished under these goals? The practical impact of the proposed research is to develop new strategies to finetune plant growth and help plants to cope with climate change. We will identify new signaling components and mechanisms by the plant photoreceptor and thermosensor phytochrome B (PHYB). The expected outcomes will enhance our understanding of how plants sense and respond to environmental light and temperature variations. In the reporting period, we reported the identification of two novel PHYB signaling components, RCB and NCP, which are required for the formation of PHYB-containing subnuclear foci named photobodies as well as photobody-associated signaling mechanisms in plant growth regulation. We also developed a new method to characterize the morphology of photobodies in response to changes in ambient temperature. Together, our work provided novel insight into the mechanisms of light and temperature signaling in plants. These breakthroughs provide the knowledge base for developing new strategies to sustain crop productivity in a changing climate.

Publications

• Type: Journal Articles Status: Published Year Published: 2019 Citation: Yoo CY, Pasoreck EK, Wang H, Cao J, Blaha GM, Weigel D, Chen M. (2019) Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat Commun 10:2629. doi: 10.1038/s41467-019-10518-0.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Yang EM*, Yoo CY*, Liu J*, Wang H, Cao J, Li F-W, Pryer KM, Sun T, Weigel D, Zhou P*, Chen M*. (2019) NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches. Nat Commun 10:2630. doi: 10.1038/s41467-019-10517-1.
• Type: Book Chapters Status: Published Year Published: 2019 Citation: Yoo CY, Williams D, Chen M. (2019) Quantitative analysis of photobodies. In: Hiltbrunner A. (eds) Phytochromes. Methods Mol Biol, vol 2026. Humana, New York, NY. doi: 10.1007/978-1-4939- 9612-4_10.