On May 19, 2024, A team led by academician Xing Wang Deng and Dr. Hang He from Peking University Institute of Advanced Agricultural Sciences (PKU-IAAS) published a paper titled "Light control of three-dimensional chromatin organization in soybean" in the Plant Biotechnology Journal. This study revealed, for the first time, the regulatory role of light in the three-dimensional chromatin organization.

 

 

The higher-order chromatin structure plays a crucial role in regulating various biological processes, including genome stability, transcriptional programs, and epigenetic modifications. However, the precise patterns and underlying mechanisms of its modulation during plant growth, development, and environmental responses remain elusive. Addressing this question, the published paper investigates the process of how plants perceive light and how it influences their growth and development, providing a new direction for understanding these phenomena.

 

Since the 1990s, prominent plant scientists such as Xing Wang Deng have conducted extensive research, culminating in the establishment of a classic theory known as the molecular mechanism of plant photomorphogenesis, focusing on multiple light signaling factors. In recent years, studies have found significant changes in chromatin compaction and genome-wide levels of histone modifications upon light exposure in plants. To systematically investigate the alterations in higher-order chromatin structure, the research team conducted Hi-C (High-throughput chromosome conformation capture) experiments on leaves, hypocotyls, and cotyledons of soybean seedlings grown under both continuous darkness and light conditions for four days. The team constructed ultra-high-resolution chromatin interaction maps, revealing that light signals enhance the strength of chromatin interactions in all tested tissues, including leaves, hypocotyls, and cotyledons.

 

Figure 1 Integration of multi-omics analysis reveals the role of higher-order chromatin structure in soybean photomorphogenesis. (a: Research system and white light spectrum of photomorphogenesis; b: Soybean photomorphogenesis phenotypes; c: Schematic diagram of multi-omics experimental design).

 

Through chromatin modification-based CUT&tag experiments, both euchromatin and heterochromatin regions were identified, with heterochromatin predominantly localized near the centromeres, accounting for 57% of the genome. Under light conditions, in addition to a general increase in heterochromatin intensity, light signals also led to interconversion between certain euchromatin and heterochromatin regions. Among the tested tissues, the hypocotyls and cotyledons exhibited the highest incidence of chromatin conversion events. Particularly noteworthy is the transformation of heterochromatin into euchromatin regions induced by light, which resulted in the activation of gene expression, including the well-known light-induced expression gene family, SAURs (Small Auxin Up-regulated RNAs).

 

Soybean genome harbors a total of 244 members in the SAURs gene family, out of which 162 genes form clusters of varying sizes within the genome, exhibiting co-expression patterns within clusters. Figure 2 illustrates a 300kb Topologically Associated Domain (TAD) containing 25 clustered SAUR genes. Upon light exposure, the TAD structures in the hypocotyls and cotyledons showed distinct compaction compared to darkness, and the co-expressed SAUR gene clusters in this tissue were activated, suggesting that TADs may mediate light-induced tissue-specific transcriptional regulation.

 

Figure 2 TADs involvement in clustered SAUR gene's tissue-specific response to light signals. (a: Changes in TAD structure composed of clustered SAUR genes under light/dark conditions; b: Transcriptional elongation of RNA Polymerase II on clustered SAUR genes under light/dark conditions; c: Tissue-specific expression of clustered SAUR genes during photomorphogenesis; d: The impact of flavopiridol (FVP), an inhibitor of RNA Polymerase II transcriptional elongation, on plant growth and development)

 

In summary, this study comprehensively investigated the regulation of chromatin higher-order structures by light signals using an integration of Hi-C, CUT&tag, and RNA-seq data, revealing the regulatory mechanisms of light-induced growth and development in different organs through three-dimensional genomic interactions.

 

This research was conducted in collaboration between ThePKU-IAAS and Tel Aviv University in Israel. Zhu Li, a jointly trained doctoral student, and Dr. Linhua Sun from ThePKU-IAAS served as co-first authors. Academician Xing Wang Deng and Dr. Hang He from ThePKU-IAAS acted as corresponding authors. Assistant researchers Xiao Xu and Yutong Liu from PKU-IAAS also contributed to this study. The research received support from the National Natural Science Foundation of China, Shandong Province Key Research and Development Program, and the Peking University Boya Postdoctoral Fellowship. The bioinformatics analysis was conducted using the high-performance computing server provided by the PKU-IAAS.

 

Paper link:

https://onlinelibrary.wiley.com/doi/10.1111/pbi.14372