Fungal genes in the innovation and evolution of land plants

ABSTRACT

Although fungal association has been instrumental to the evolution of land plants, how genes of fungal origin might have contributed to major plant innovations remains unclear. In a recent study, we showed that a macro2 domain-containing gene likely acquired from mycorrhiza-like fungi is important in gametophore development of mosses, suggesting a role of fungi-derived genes in the three-dimensional growth of land plants.

Symbiosis between plants and fungi is critical for the evolution and adaptation of land plants.^1,2 Particularly, mycorrhizae (fungi-root association) occur in all major groups of vascular plants, and mycorrhiza-like structures are also found in liverworts and hornworts, two major groups of nonvascular plants.^3,4 This association between plants and fungi improves nutrient utilization, drought, and pathogen resistance in plants.^5,6 Other than this mutualistic partnership, fungi are also present in almost all land plants in the form of pathogens, parasites, endophytes, or epiphytes. For instance, mosses are often associated with parasitic and endophytic fungi, even though they are not known to have mycorrhiza-like structures;^4,7 the lack of mycorrhiza-like fungi, however, is generally considered to be a secondary loss, as the ancestors of mosses most likely had a mycorrhiza-like fungal association.⁵

Given the intimate and long-term association between fungi and land plants, the exchange of nutrients and genetic material may occur between the two partners. Horizontal gene transfer (HGT) is a process of genetic material exchange between distinct species. Novel genes (or functions) acquired through HGT may allow recipient organisms to better adapt to their environments or to access new niches and resources. Although widely regarded as a driving force in prokaryotic evolution,⁸ HGT from fungi to land plants, especially nonvascular land plants (i.e., bryophytes, including liverworts, mosses, and hornworts), has also been reported in recent years, and many of the reported genes are related to the development and stress response of land plants.^9–16 For instance, fungal hemerythrin gene was transferred to bryophytes, where it participates in oil body biogenesis and dehydration resistance in mosses.¹² Two large genomic regions containing mostly fungi-specific genes were found in the moss Physcomitrium patens (formerly Physcomitrella patens¹⁷), suggesting that HGT from fungi to plants might occur either frequently or in large fragments; the acquired fungal genes might have contributed to the defense of mosses against fungal or other microbial pathogens.¹⁴ These genes likely resulted from either fungal symbiosis with the ancestors of mosses or other scenarios such as parasitism.^4,9,14 Recently, a rare HGT event from fungi to grasses, involving Fusarium head blight resistance gene Fhb7, was reported.¹⁸ Fhb7 was acquired by wheatgrasses (Thinopyrum spp.) from fungal endophytes, and it was later artificially introduced to wheat through hybridization to improve Fusarium resistance and crop yields. While many of the acquired fungal genes in land plants are related to biotic or abiotic stress responses,⁹ whether and how fungal genes may contribute to major innovations of land plants have rarely been documented.

One of the major innovations in land plants is three-dimensional growth. In mosses, the three-dimensional growth is primarily represented by gametophores. In a recent study,¹³ we found that a macro2 domain-containing gene of fungal origin plays a significant role in stem cell and gametophore development in mosses. This macro2 domain-containing gene was likely acquired from mycorrhiza-like fungi, mostly the fungal group Mucoromycota, to the ancestral land plant and selectively retained in bryophytes. In P. patens, this gene (PpMACRO2) is expressed mainly in stem cells based on GUS staining, especially in apical stem cells of buds and gametophores (Figure 1a-c). Considering the strong expression of PpMACRO2 in stem cells, tissue regeneration from detached leaves was performed in vitro, and strong GUS expression was observed in regenerated protonemal filaments (Figure 1d). To further understand the functions of PpMACRO2, we generated knockout and over-expression mutants of PpMACRO2, respectively. Compared to the wild-type (WT), the knockout lines (ppmacro2) produced larger gametophores, whereas the over-expression lines (PpMACRO2-OE) had smaller gametophores (Figure 1e). These results show that PpMACRO2 regulates stem cell function, cell reprogramming, gametophore development, and other processes in P. patens. Furthermore, these data indicate that fungi could donate genes to their plant partners and contribute to the structural and physiological innovations of land plants.

Figure 1.

Mycorrhizae-like gene PpMACRO2 affects stem cell and gametophore development in P. patens. (a) Protonema tip stem cell. (b) Three-faced bud. (c) Gametophore. (d) Tissue regeneration from detached leaves. (e) Gametophore development from four-week-old WT, ko and OE plants of PpMACRO2. Scale bar: 100 μm in a-d; 500 μm in e

With the rapid advancement of sequencing technology, an increasing amount of genomic data has become available for various plant groups, thus providing an unprecedented opportunity to understand the role of HGT in plant evolution. Other than their role in plant development, fungal genes could also have applications in crop improvement and biotechnology, as indicated by the study of Fhb7.^18,19 Particularly, given the role of acquired fungal genes in the stress resistance of plants, as shown by the available studies,^9–12,14 we expect that some of these acquired fungal genes might be utilized in crop breeding and improvement.

Funding Statement

This work is funded in part by the National Natural Science Foundation of China (31970248), and the Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (2019QZKK0502).

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.