Multi-omics analysis reveals spatiotemporal regulation and function of heteromorphic leaves in Populus

Abstract

Despite the high economic and ecological importance of forests, our knowledge of the adaptive evolution of leaf traits remains very limited. Euphrates poplar (Populus euphratica), which has high tolerance to arid environment, has evolved four heteromorphic leaf forms, including narrow (linear and lanceolate) and broad (ovate and broad-ovate) leaves on different crowns. Here, we revealed the significant functional divergence of four P. euphratica heteromorphic leaves at physiological and cytological levels. Through global analysis of transcriptome and DNA methylation across tree and leaf developmental stages, we revealed that gene expression and DNA epigenetics differentially regulated key processes involving development and functional adaptation of heteromorphic leaves, such as hormone signaling pathways, cell division, and photosynthesis. Combined analysis of gene expression, methylation, ATAC-seq and Hi-C-seq revealed longer interaction of 3D genome, hypomethylation, and open chromatin state upregulates IAA-related genes (such as PIN-FORMED1 and ANGUSTIFOLIA3) and promotes the occurrence of broad leaves while narrow leaves were associated with highly concentrated heterochromatin, hypermethylation and upregulated ABA pathway genes (such as Pyrabactin Resistance1-like10). Therefore, development of P. euphratica heteromorphic leaves along with functional divergence was regulated by differentially expressed genes, DNA methylation, chromatin accessibility, and 3D genome remodeling to adapt to the arid desert. This study advances our understanding of differential regulation on development and functional divergence of heteromorphic leaves in P. euphratica at the multi-omics level and provides a valuable resource for investigating the adaptive evolution of heteromorphic leaves in Populus.

Comparative genomic analysis of the Growth-Regulating Factors-Interacting Factors (GIFs) in six Salicaceae species and functional analysis of PeGIF3 reveals their regulatory role in Populus heteromorphic leaves

“…Each type of heteromorphic leaves with different leaf ages was replicated three times for sampling. The napkin was used to delicately clean the leaves, which were then rapidly frozen in liquid nitrogen and stored at an ultra-low temperature of -80℃ in a refrigerator for RNA-seq analysis (the dataset has been made available to the public for access [ 7 ] and preservation through the National Genomics Data Center ( https://ngdc.cncb.ac.cn/ ), under project number PRJCA005959.…”

“…In particular, Populus euphratica characterized by its extraordinary tolerance to drought and salinity, serves as a pivotal species in desert oases and stands out as an exceptional relic plant thriving in extremely arid environments [ 5 , 6 ]. P. euphratica exhibits a distinct pattern of leaf heteroblasty, with adult trees displaying a sequential production of linear (Li, leaf index ≥ 4), lanceolate (La, 2 ≤ leaf index < 4), ovate (Ov, 1 ≤ leaf index < 2), and broad ovate (Bo, leaf index < 1) leaves as they ascend from the lower canopies to the upper canopies, accompanied by a gradual increase in leaf width and area [ 7 ]. Previous research indicated that broad Ov and Bo leaves in P. euphratica exhibit greater resilience to drought than narrow Li and La leaves, as evidenced by their thicker palisade tissue and enhanced photosynthetic activity [ 8 ].…”

Comparative genomic analysis of the Growth Regulating Factors-Interacting Factors (GIFs) in six Salicaceae species and functional analysis of PeGIF3 reveals their regulatory role in Populus heteromorphic leaves

“…Each type of heteromorphic leaves with different leaf ages was replicated three times for sampling. The napkin was used to delicately clean the leaves, which were then rapidly frozen in liquid nitrogen and stored at an ultra-low temperature of -80℃ in a refrigerator for RNA-seq analysis (the dataset has been made available to the public for access [34] and preservation through the National Genomics Data Center (NGDC, https://ngdc.cncb.ac.cn/), under project number PRJCA005959).…”

Morphological, Anatomical, and Physiological Characteristics of Heteroblastic Acacia melanoxylon Grown under Weak Light

“…Many genes related to hormone regulation pathways and environmental stress have been screened out in P. euphratica [ 8 , 9 ], Juniperus flaccida , Pinus cembroides [ 10 ], and some aquatic plants [ 11 ], which are essential in regulating vascular development, stomatal morphology, leaf polarity, and epidermal cell differentiation. Recent studies have employed multi-omics analysis to investigate the regulation and function of heteromorphic leaves [ 12 ]. Nevertheless, the exact mechanism of heteromorphic leaves formation has yet to be elucidated.…”