True morels (Morchella, Pezizales) are a popular edible and medicinal fungus with great nutritional and economic value. The dynamics and regulatory mechanisms during the morphogenesis and maturation of morels are poorly understood. In this study, the metabolomes and transcriptomes of the mycelium (MY), primordium differentiation (PR), young fruiting body (YFB), and mature fruiting body (MFB) were comprehensively analyzed to reveal the mechanism of the morphogenesis and maturation of Morchella sextelata. A total of 748 differentially expressed metabolites (DEMs) and 5342 differentially expressed genes (DEGs) were detected, mainly enriched in the carbohydrate, amino acid, and lipid metabolism pathways, with the transition from the mycelium to the primordium being the most drastic stage at both the metabolic and transcriptional levels. The integrated metabolomics and transcriptomics highlighted significant correlations between the DEMs and DEGs, and specific amino acid and nucleotide metabolic pathways were significantly co-enriched, which may play key roles in morphological development and ascocarp maturation. A conceptual model of transcriptional and metabolic regulation was proposed during morphogenesis and maturation in M. sextelata for the first time, in which environmental factors activate the regulation of transcription factors, which then promote metabolic and transcriptional regulation from vegetative to reproductive growth. These results provide insights into the metabolic dynamics and transcriptional regulation during the morphogenesis and maturation of morels and valuable resources for future breeding enhancement and sustainable artificial cultivation.

The genetic control of plant architecture in crops is critical for agriculture and understanding morphological evolution. This study showed that an open reading frame (ORF) of the rice domestication gene PROG1 appeared 3.4–3.9 million years ago (Mya). Subsequently, it acquired a novel protein-coding gene function in the genome of O. rufipogon (~0.3–0.4 Mya). This extremely young gene and its paralogous C2H2 genes located nearby define the prostrate architecture of O. rufipogon and, thus, are of adaptive significance for wild rice in swamp and water areas. However, selection for dense planting and high yield during rice domestication silenced the PROG1 gene and caused the loss of the RPAD locus containing functional C2H2 paralogs; hence, domesticated lines exhibit an erect plant architecture. Analysis of the stepwise origination process of PROG1 and its evolutionary genetics revealed that this zinc-finger coding gene may have rapidly evolved under positive selection and promoted the transition from non- or semi-prostrate growth to prostrate growth. A transgenic assay showed that PROG1 from O. rufipogon exerts a stronger function compared with PROG1 sequences from other Oryza species. However, the analysis of the expression levels of PROG1 in different Oryza species suggests that the transcriptional regulation of PROG1 has played an important role in its evolution. This study provides the first strong case showing how a fundamental morphological trait evolved in Oryza species driven by a gene locus.

Morels (Morchella spp.), as one of the rare macroascomycetes that can be cultivated artificially, possess significant economic and scientific values. Morel cultivation is highly sensitive to elevated temperatures; however, the mechanisms of their response to heat shock remain poorly understood. This study integrated transcriptomic and quantitative proteomic analyses of two M. sextelata strains with different thermotolerance (labeled as strains C and D) under normal (18 °C) and high temperature (28 °C) conditions. From over 9300 transcripts and 5000 proteins, both consistency and heterogeneity were found in response to heat shock between the two strains. Both strains displayed a capacity to maintain cellular homeostasis in response to heat shock through highly expressed cell wall integrity (CWI) pathways, heat shock proteins (HSPs), and antioxidant systems. However, strain D, which exhibited stronger thermotolerance, specifically upregulated the ubiquitin ligase Rsp5, thereby further promoting the expression of HSPs, which may be a key factor influencing the thermotolerance difference among M. sextelata strains. A conceptual model of the heat shock adaptation regulatory network in M. sextelata was proposed for the first time; the results provide novel insights into the thermotolerance response mechanisms of macroascomycetes and valuable resources for the breeding enhancement of thermotolerant morel strains.