A cross-species co-functional gene network underlying leaf senescence

Abstract

The complex leaf senescence process is governed by various levels of transcriptional and translational regulation. Several features of the leaf senescence process are similar across species, yet the extent to which the molecular mechanisms underlying the process of leaf senescence are conserved remains unclear. Currently used experimental approaches permit the identification of individual pathways that regulate various physiological and biochemical processes; however, the large-scale regulatory network underpinning intricate processes like leaf senescence cannot be built using these methods. Here, we discovered a series of conserved genes involved in leaf senescence in a common horticultural crop (Solanum lycopersicum), a monocot plant (Oryza sativa), and a eudicot plant (Arabidopsis thaliana) through analyses of the evolutionary relationships and expression patterns among genes. Our analyses revealed that the genetic basis of leaf senescence is largely conserved across species. We also created a multi-omics workflow using data from more than 10 000 samples from 85 projects and constructed a leaf senescence-associated co-functional gene network with 2769 conserved, high-confidence functions. Furthermore, we found that the mitochondrial unfolded protein response (UPR^mt) is the central biological process underlying leaf senescence. Specifically, UPR^mt responds to leaf senescence by maintaining mitostasis through a few cross-species conserved transcription factors (e.g. NAC13) and metabolites (e.g. ornithine). The co-functional network built in our study indicates that UPR^mt figures prominently in cross-species conserved mechanisms. Generally, the results of our study provide new insights that will aid future studies of leaf senescence.

Acknowledgements

This research was sponsored by the National Natural Science Foundation of China (32071160; 32161133021; 32101682), Shanghai Association for Science and Technology (20ZR14279; 20YF1422000), and Shanghai Jiao Tong University (20X100040052). We thank TopEdit (www.topeditsci.com) for linguistic assistance during the preparation of this manuscript.

Author contributions

M.-Y.L. planned and designed the research. M.-Y.L. and C.-C.G. analyzed the data. M.-Y.L. wrote the original manuscript. K.-X.X. and K.C. determined the expression of genes by qRT–PCR. K.-X.X. and Y.-D.W. measured the chlorophyll content. C.-C.G., J.-H.C., and K.C. used the method to integrate plant data. X.W. reviewed and edited the manuscript. M.-Y.L., J.-H.C., and Y.-D.W. revised the manuscript. X.W. and Y.-D.W. supervised the research. All authors read and approved the final manuscript.

Data availability

All RNA-seq data were deposited at NCBI under GEO Series GSE201607, Sample accession numbers GSM6068492-GSM6068509, and Experiment/Run accession number SAMN27783488-SAMN27783505.

Conflict of interest

The authors have no conflict of interest to declare.

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