During leaf senescence, the final stage of leaf development, nutrients are recycled from leaves to other organs, and therefore proper control of senescence is critical for plant fitness. Although substantial progress has been achieved in understanding leaf senescence in annual plants, the molecular factors that control leaf senescence in perennial woody plants are largely unknown.

On February 6, Chair Professor Hongwei Guo from the Department of Biology at the Southern University of Science and Technology (SUSTech) led his research team to publish a paper in the prestigious botany journal The Plant Cell. Their article, entitled “An Alternative Splicing Variant of PtRD26 Delays Leaf Senescence by Regulating Multiple NAC Transcription Factors in Populus,” showed a novel mechanism underlying the alternative splicing control of leaf senescence.

Leaf senescence is the last stage of leaf development and is characterized by the transition from nutrient assimilation to remobilization. Therefore, leaf senescence has been regarded as a genetically controlled developmental process that is evolutionarily acquired for better fitness and survival. Substantial progress has been made in describing leaf senescence at the molecular level through the characterization of hundreds of senescence-related mutants and the identification of thousands of senescence-associated genes (SAGs) through multi-omics technologies in annual plants. As a natural phenomenon in temperate deciduous trees, autumn leaf senescence attracts wide public attention every year. However, the molecular factors that control leaf senescence in perennial woody plants remain unclear.

In this study, RNA sequencing was performed to obtain a high-resolution temporal profile of gene expression during autumn leaf senescence in Populus tomentosa, an indigenous tree species that plays a key role in the establishment of plantation forests along the Yellow River in China. Unsupervised hierarchical clustering of differential gene expression profiles identified 3,459 autumn senescence-associated genes (ASAGs). Identification of hub transcription factors (TFs) by co-expression network analysis of ASAGs revealed that NAC family TFs play important roles in regulating autumn leaf senescence. Interestingly, an intron retention (IR) event in the mRNA of a NAC TF, PtRD26, caused by alternative splicing (AS), was found to occur in an age-dependent manner and result in a truncated protein PtRD26^IR. PtRD26^IR functions as a dominant-negative regulator of leaf senescence by physically interacting with PtRD26 and other homologous NAC TFs, thereby repressing their DNA binding activity. Functional analysis of senescence-associated splicing factors revealed that U2 auxiliary factors U2A2A and U2A2B are involved in AS of PtRD26^IR. Correspondingly, silencing of U2A2A or/and U2A2B decreases PtRD26^IR transcript abundance and induces early senescence in poplar leaves. This work provides new insights into the molecular mechanisms controlling leaf senescence in trees.

A proposed model illustrating senescence-associated alternative splicing of PtRD26 in the regulation of Autumn leaf senescence

Dr. Hou-Ling Wang and Dr. Yi Zhang, two postdoctorals from the Beijing Forestry University (BFU), are the co-first authors. Professor Hongwei Guo and Dr. Zhonghai Li are the co-corresponding authors. SUSTech engineer Dr. Xing Wen, Assistant Professor Enyang Li, and Bosheng Li from the Institute of Plant and Food Science, are the co-authors.

This work was funded by the National Natural Science Foundation of China (NSFC), Shenzhen Science and Technology Program, Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes (SUSTech), and the startup funding for plant aging research from the Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University.

Paper link: https://academic.oup.com/plcell/advance-article/doi/10.1093/plcell/koab046/6129781?searchresult=1