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. 2024 Apr 29;13(9):1233.
doi: 10.3390/plants13091233.

Fungal Hyphae on the Assimilation Branches Are Beneficial for Haloxylon ammodendron to Absorb Atmospheric Water Vapor: Adapting to an Extreme Drought Environment

Xiaohua Wang  1 , Honglang Xiao  1 , Lei Pang  2 , Fang Wang  1
Affiliations

Fungal Hyphae on the Assimilation Branches Are Beneficial for Haloxylon ammodendron to Absorb Atmospheric Water Vapor: Adapting to an Extreme Drought Environment

Xiaohua Wang et al. Plants (Basel). .

Abstract

Research on endophytic fungi in desert plants, particularly the epiphytic or endophytic fungi of leaves, remains limited. In the extremely arid regions of northwest China, the ultra-xerophytic desert plant Haloxylon ammodendron harbors white fungi on its assimilating branches during autumn. The hyphae of these fungi intertwine, both internally and externally, comprising superficial, bridging, and endophytic types. The superficial hyphae attach to the surface of the assimilating branches and continuously grow and intersect, forming a thick layer of felt-like hyphae. This thick, felt-like layer of hyphae facilitates the adsorption of atmospheric water vapor on the surface of the hyphae or the assimilating branches, allowing H. ammodendron to capture atmospheric moisture, even under low humidity. Some superficial hyphae penetrate the cuticle into the epidermis, becoming bridging hyphae, which can rapidly transport water from the outside of the epidermis to the inside. The endophytic hyphae shuttle within the epidermis, achieving rapid water transfer within the epidermis of the assimilating branches. The presence of these three types of hyphae not only enables the assimilating branches of H. ammodendron to achieve rapid water absorption and transmission, but also facilitates the uptake of atmospheric water vapor under low humidity conditions. We discuss the mechanism by which the hyphae promote water absorption from the perspectives of hyphal composition, the formation of felt-like structures, and environmental conditions. We consider the presence of fungal hyphae on the surface of the H. ammodendron assimilating branches as an inevitable ecological process in arid environments. This study provides important theoretical insights into the mechanisms underlying the strong drought resistance of desert plants in extremely arid regions and offers strategies for desertification control.

Keywords: Haloxylon ammodendron; assimilation branches; atmospheric water vapor absorption; drought adaptability; fungal hyphae.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
White hyphae on the surface of Haloxylon ammodendron assimilating branches ((A,B), no hyphae; (C–E), a small amount of white hyphae; (F,G) an abundance of white hyphae).
Figure 2
Figure 2
Infiltration laws of the fungus and its morphological identification. (A–D), the patterns of fungal infiltration of assimilation branches of Haloxylon ammodendron; (A), Haloxylon ammodendron assimilation branches been infiltrated by the fungus with white felt-like hyphae, the yellow arrows point light yellow edematous patches at the early stage of fungal infection, the red arrows point yellowish brown to brown cleistothecium at the late stage of fungal infection; (B), at the early stage of fungal infiltration, yellowish dots existing in the white hyphae on the assimilation branches; (C), enlarged light yellow edematous patches in the yellow box in (A); (D), enlarged yellowish brown to brown cleistothecium in the red box in (A); (E–H), the morphological identification of the fungus; (E), the cleistothecium embedded in the hyphae (indicated by the white arrow); (F), the enlarged cleistothecium; (G), the conidium growing out of stomata; (H), the red arrow indicates the primary conidium, and the white arrow indicates the secondary conidium. The line represents 20 µm.
Figure 3
Figure 3
Structural characteristics of hyphae outside or inside the epidermis of assimilation branches of Haloxylon ammodendron. (A–E), hyphae surface images. (A), bright field optical image under natural conditions; (B), fluorescence image corresponding to (A); (C–E), fluorescence surface images after absorption of FB fluorescent reagent in the fluorescence humidification experiment; (F–I) cross-sectional fluorescence images after absorption of FB fluorescent reagent in the fluorescence humidification experiment; (H), the magnification at the yellow box of (G), and the white arrow indicates the cross section of the hyphae. PC, primary conidium; SC, secondary conidium; Cl, cleistothecium; Hy, hyphae; St, stomata.
Figure 4
Figure 4
Comparison of water content and water potential of assimilation branches, with and without hyphae, during the ultrapure water humidification. (A,B), the temperature and relative humidity in the humidification experiment room and in the natural atmospheric environment; (C), change in water content (%); (D), change in water potential (MPa); (E), change in water content during a time period (%); (F), change in water potential during a time period (MPa). Data were organized by Office Excel 2016, and statistical analysis was performed using R language (R version 4.3.2) software employing the Wilcoxon test method: *, p < 0.05; **, p < 0.01; and ns, no statistically significant difference. In (C–F), A in the legend indicates assimilation branches without hyphae, and B indicates assimilation branches with hyphae.
Figure 5
Figure 5
Comparison of water absorption of fluorescence humidification between assimilation branches, with hyphae and without hyphae. (A) Comparison of indoor and outdoor temperature and humidity for fluorescent humidification. (B) Comparison of the fluorescence emitted by hyphae on Haloxylon ammodendron assimilation branches under different fluorescence humidification durations. The duration of fluorescence humidification for (a), (b), and (c) was about 0.5 h, 1.5 h, and 3 h, respectively. (d) A complete cross-sectional fluorescence comparison of hyphae or hyphae-free parts of the same assimilation branch; (e) enlargement of the yellow box in the area with hyphae in (d); (f) magnification of the red box at hyphae-free site of (d).
Figure 6
Figure 6
Comparison of absorption of atmospheric water vapor by assimilation branches of Haloxylon ammodendron, with hyphae and without hyphae, under different fluorescence humidification durations. (A,C,E) were used for assimilating branches without hyphae for about 0.5 h, 1.5 h, and 4.5 h, respectively. (B,D,F) were used for assimilating branches with hyphae at about 0.5 h, 1.5 h, and 4.5 h, respectively.
Figure 7
Figure 7
Comparison of water transport pathways between the epidermis of assimilation branches of Haloxylon ammodendron, with hyphae and without hyphae, under the same humidification conditions. (A,C,E) Transport routes of water in the epidermis with hyphae in assimilation branch after humidification for 1.5 h. (B,D,F) Transport routes of water in the epidermis of no-hyphae branches for about 3–4.5 h humidification. The white arrow indicates the hyphae, the red arrow indicates the cuticle, and the yellow arrow indicates the cross section of the hyphae in the epidermis. Sv, small vascular bundle; Cr, crystalline cells.
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