In soil around roots that hosts to plant secretions, root-infecting fungi named mycorrhizae are the dominant organisms. Most mycorrhizal root infections operate as a mutualism, with the plant providing the fungus with energy for respiration in return for minerals and resources that would be otherwise more difficult to access in soil. The relationships between a plant and its mycorrhizae can significantly affect the growth, survival, and fitness of the plant. In the set of tree species for the FOR305 ID Test, there are two functionally distinct types of mycorrhizae—vesicular-arbuscular mycorrhizae (VAM), which penetrate the root’s cell wall and Ectomycorrhizae (ECM), which do not. This study examines the relationship between the species found on the ID Test, and their mycorrhizal “status,” i.e. whether they are most commonly infected by VAM, ECM, both, or none. All species that have significant nutrient limitations have a mycorrhizal infection of some type, predominantly VAM. ECM infections are dominant.in species that range into more stressful habitats where drought or critical nutrient deficiencies are challenges, such as the Boreal region.
Mycorrhizae Physiology and Ecology
The two mycorrhizal types examined in this paper are defined structurally. Vesicular-Arbuscular Mycorrhizae are formed by glomeromycetous fungi. VAM create arbuscles – branched exchange structures – inside the root, notably penetrating the walls of interior root cells (Bagyaraj, 1991; Wang et. al., 2006). Ectomycorrhizae are formed by basidiomycetous and ascomycetous fungi, and create exchange structures known as Hartig nets between cortical root cells. Hartig nets do not penetrate cell walls (Mukerji et. al. 1991). ECM are generally exclusive to perennials, a relationship attributed to the success of perennials in low nutrient, disturbed, and stressful habitats (Trappe, 1987).
Mycorrhizae can benefit plants in a range of ways.In general, mycorrhizae have the ability to gain resources that plants cannot adequately access. Because they have a smaller diameter than that of root hairs, fungal hyphae are better able to colonize pores in the soil (Allen, 1991). As noted by Eissenstat, a smaller diameter means a higher length:root mass ratio, which is generally beneficial, as root uptake is primarily correlated with length rather than mass (1992). Benefits are not always constant over the life of the plant. For some species, mycorrhizal infections have a negligible effect, except in times of resource stress, most often drought (Allen, 1991). In these cases, the mycorrhizae are not a continual mutualistic partner, but an “insurance policy.” Mycorrhizae can also be important during early development, giving seedlings a readily accessible network of resources (Allen, 1991). This is especially true if the surrounding plants are closely related, as networks of mycorrhizae between hosts have been shown to allow nutrients to transfer in any direction, and in a way which prefers hosts which are most genetically similar to other hosts in the network (Dighton, 2003).
Evolutionary History of Mycorrhizae
Most of the literature which summarizes mycorrhizal status does so in relation to the evolutionary history of mycorrhizae. Both Trappe (1987) and Wang (2006) overlaid mycorrhizal status information with phylogenies to examine the change of mycorrhizal status as plants evolved. The colonization of land plants coincided with the evolution of the ancestor of VAM, and it is thought that colonization on land would not have been possible without fungal symbiosis (Trappe, 1987). Glomeromycetous (VAM) species occur in early plant lineages, and are thus common, in contrast to ascomycetous and basidiomycetous (ECM) species, for which the earliest fossil records are much younger (Wang et. al., 2006). This trend – VAM infections being ancestral and common, and ECM infections being more recent and rarer – is homologous between vascular and non-vascular plants, indicating that it is a trend for plant species in general (Wang et. al., 2006). Trappe (1987) notes that the more archaic plant clades in which VAM associations are found are generally characterized by root structures with minimal root hairs, and that ECM-associated clades tend to have more prolific root hair growth. While this may be true for plants overall, the data corresponding to diameter of laterals (highest order root tissue) from Eissenstat (1992) is inconclusive in the ID Test species group (Table 1).
|Species||Diameter (µm)||Family Mycorrhizal Status|
Table 1. Diameter of Laterals (Eissenstat, 1992), and Mycorrhizal Status (Wang et. al., 2006). aSpecies is an ID Test species. bFamily of species is the same as an ID Test species family.
Over evolutionary history, mycorrhizal status of a species converts from VAM-associated to more “advanced” statuses, such as ECM-associated, on many independent occasions (Wang et. al., 2006). Wang describes the strategy of ECM association as short-term, an opportunistic response to more strenuous environmental conditions, which explains why there are many independent conversions to ECM association, and yet VAM association is still dominant.
Despite the dominance of VAM association, Trappe (1987) suggests that the evolutionary trajectory for plants is toward more advanced associations such as ECM, and eventually to complete independence from any mycorrhizal association, with the caveat that “we won’t know for a million years” (23).
State of Mycorrhizal Status Research
Research efforts to catalogue mycorrhizal status have been cumulative, with newer papers and databases building on earlier work. The first large-scale summaries of studies on mycorrhizal status of individual species were performed by J.M. Trappe on angiosperms and by Harley and Harley on British flora, both in 1987. Trappe defined associations down to the scale of orders. Subsequent work by Wang et. al. in 2006 cited Trappe extensively, but added information from additional studies and further defined associations down to the scale of families, and included specific associations for the species used. Furthermore, Wang et. al. used a more complete and up-to-date phylogeny in their analysis, which increased the depth of evolutionary analysis with regards to associations. Hempel (2013) created a species-specific association list which cited Wang et. al. extensively, a recovered study performed by Akhmetzanova et. al. (2012) from the former Soviet Union, and additional new studies.
The reliability of such studies varies—as noted by Trappe (1987), the more a species is studied, the more likely it is that it will have a more complex association, with multiple mycorrhizal types, or with instances where the host is autotrophic and does not have an association. Only about 3% of all land species have had their associations studied, and these are predominantly species with high commercial value (Wang et. al., 2006).
Future studies are likely to continue building on previous work, adding new records from understudied groups, such as mosses, and improving on past analysis hand-in-hand with improvements to plant phylogenies (Wang et. al., 2006).
Ecological Characteristics of ID Test Hosts Related to Mycorrhizal Status
The species from the Tree ID test form three distinct groups of mycorrhizal associations (Figure 1). By family, species tend to be either obligately ECM-infected, obligately VAM-infected, or obligately mycorrhizal and with multiple possible associations (Table 2). There were no strong tendencies towards facultative associations–the family with the strongest tendency towards being facultatively mycorrhizal was Juglandaceae, and only one out of the three species studied in this family by Wang et. al. (2006) were facultatively mycorrhizal. The exception to this is Celtis occidentalis, which was a strong outlier. Similarly, no family was strongly non-mycorrhizal. The strongest non-mycorrhizal status was in the Magnoliaceae family, with one out of the tree species studied by Wang et. al. being nonmycorrhizal. Thus, the Tree ID set as a whole was found to be obligately mycorrhizal.
Species and Familes Exclusive to Vesicular – Arbuscular Mycorrhizae
The most prominent orders that were found to be obligate to VAM were the Sapindales, Rosales, Magnoliales, Pinales, and Fabales (Table 2). As noted by both Trappe and Wang, VAM associations are dominant among species. The ID Test set followed this trend, with VAM associations being the most common among families. Trappe (1987) hypothesized that the Magnolia genus retained more VA M because it had more primitive traits. Since the ancestor to VAM is thought to have been a key innovation which allowed the evolution of land plants, this would suggest that more primitive groups of species would be more dependent on VAM assocations. Any other species group that showed similarly primitive traits, specifically root hairs that are coarse and sparse, is likely to have a strong VAM association to help improve nutrient intake (Bagyaraj, 1991). This is supported by the findings of Smith and Read (2008), who showed that VAM roots were often more efficient in nutrient acquisition per unit length than non-infected roots.
VAM hosts are geographically ubiquitous, and grow in arctic and temperate regions (Bagyaraj, 1991). However, no VAM host for which there was USDA tree range data was found to grow in the arctic region (Appendix A-1). This suggests that there may be limitations to VAM associations with trees in the arctic region.
Chalot and Plassard (2012) noted that VAM play a major role in increasing nutrient uptake, especially for phosphorus, but have limited capacity to release nitrogen or phosphorus from inorganic forms. Conversely, ECM can actively take up inorganic nutrients and provide them to the host. From this, it can be seen that VAM and ECM provide nutrients to their hosts in functionally different ways. If the more “passive” provision of nutrients from VAM were not adequate for the needs of polar region trees, then any VAM association would be less beneficial, possibly even to the point of creating a parasitic relationship where the fungus would acquire carbon at the expense of the host. Since negative effects of mycorrhizae, especially early on in the field, were ignored or suppressed, the mutualism-parasitism continuum of mycorrhizal associations were unrecognized (Smith and Read, 2008). Trade-offs with mycorrhizal associations may explain the lack of polar-region VAM trees, but these relationships need to be further explored.
Species and Families exclusive to Ectomycorrhizae
The most prominent orders that were found to be obligate to Ectomycorrhizae were the Pinales and Fagales (Table 2). This is consistent with the findings of Wang et. al. (2005), who showed that Pinaceae and Fagales were dominantly ECM obligate. From analyzing the numerous instances when ECM associations evolved, Wang et. al. hypothesize that the majority of ECM hosts typically grow in nutrient-poor environments, and descend from clades that used to live in less stressful environments; for example, Rosids such as the Malvales. Ectomycorrhizae are known to sometimes have associations with nitrogen-fixing bacteria, which would help in the colonization of areas with resource limitations (Trappe, 1987).
Aside from living in more limited environments, ECM hosts tend to be dominant later in succession, due to greater efficiency in nutrient extraction (Trappe, 1987). As noted earlier, Ectomycorrhizae are more active in nutrient intake. They are also known to secrete enzymes to break down the litter layer in order to gain better access to nutrients (Chalot and Plassard, 2012). Furthermore, while VAM are known to branch into a fan-shaped pattern, the outer extent of ECM, the mycelium, forms a net-shaped structure, which allows for better substrate colonization (Allen, 1991).
For trees in temperate and boreal regions, much of the nitrogen needed for growth comes from nutrient turnover, the decomposition of dead organic matter (Chalot and Plassard, 2012). Since ECM are effective scavengers, northern trees can benefit from having an ECM network to increase the availability of nitrogen in such systems. While associating with an actively scavenging host may be beneficial in temperate and boreal regions, especially where there are nutrient limitations, the cost of such associations may be prohibitive in more generous environments, explaining why VAM associations remain dominant.
Analysis of USDA tree range data for ECM hosts shows that they span both Polar and Temperate domains (Appendix A-2). ECM host ranges in temperate regions were more limited than the range of VAM hosts, perhaps as a result of being outcompeted in good conditions.
Species and Families Which Are Flexible or Dual Symbionts
The two families which displayed flexibility in association were Salicaceae and Juglandaceae. This is consistent with Trappe (1987), who noted that Salicaceae tend to be very flexible in mycorrhizal associations.
Analysis of USDA tree range data shows that species with flexible associations largely range in the intersection of VAM and ECM ranges, except for Populus Tremuloides. While the Salicaceae family shows flexible associations, P. Tremuloides (Trembling Aspen) is specifically exclusive to ECM (Wang et. al., 2005), and as such shows a distribution similar to other ECM-associated species, with a large range in the polar domain.
The mycorrhizal status of the species examined was dominantly obligative, with associations with Vesicular-Arbuscular Mycorrhizae being common, associations with Ectomycorrhizae being secondary, prevalent especially in species that range in nutrient limited conditions, and with a small group of species that displayed flexible associations. For the most part, facultative associations or the absence of associations were sporadic and minor in the families from the Tree ID test.
The defining characteristic of trees is the extensive production of woody tissue, an undertaking which requires good access to nutrients. It is not surprising then that most trees have mycorrhizal associations, as these mutualisms tend to improve nutrient access. The most influential factor for determining VAM versus ECM status seems to be environmental stress, a hypothesis which is supported by the many parallel occurrences of ECM status corresponding to nutrient stress found by Wang et. al. (2006). From the ranges analyzed in this paper and current knowledge of the differences between VAM and ECM fungi, it seems that resource trade-offs play an important role in determining the success of both types of associations. Therefore, through various mechanisms, environment is the main factor which determines mycorrhizal status in trees.
There is much more research to be done examining mycorrhizal status for individual species. Even for a set of well-known species, such as the ones used in this study, information on status at the species level is fairly incomplete, and relies on a limited number of observations. The scale of work required to create a comprehensive database will require a continuous and worldwide effort. More work also needs to be done on mycorrhizal associations through the lens of the mutualism-parasitism gradient, to determine how associations affect the realized niche of individual species. Due to limited sampling, our current understanding of broad-scale patterns of mycorrhizal association is likely to be too simplistic. The future of mycorrhizae and their hosts will be more complicated, which makes it all the more worthwhile to explore.
Table 2. Mycorrhizal Status of Species and Families from the ID Test set. Status: Association of species with mycorrhizae, according to Wang et. al., 2006, or Hempel et. al., 2013 (VAM: Obligate with Vesicular-Arbuscular Mycorrhizae, NM: Non-Mycorrhizal (Autotrophic), ECM: Obligate with Ecomycorrhizae). Family: family of species. n=number of species sampled in family. M%: % of family that is obligately mycorrhizal. FM%: % of family that is facultatively mycorrhizal. NM%: % of family that is non-mycorrhizal. VAM: % of family that associates with VAM. ECM: % of family that associates with ECM. Both: % of family that associates with VAM and ECM concurrently. Other: % of family that associates with other mycorrhizal types and combinations. Columns “Family” to “Other” all from Wang et. al., 2006.
Appendix A – Distribution Maps
Make up paper appendix a (PDF)
Ecoregions data (ArcGIS shapefiles) from Bailey, 2003.
Species Range data (ArcGIS shapefiles) from US Geological Survey, 1999.
Species used in Appendix A-1 (n=17)
Acer negundo (Manitoba Maple)
Acer rubrum (Red Maple)
Acer saccharinum (Silver Maple)
Aesculus glabra (Ohio Buckeye)
Asimina triloba (Paw‐Paw)
Celtis occidentalis (Hackberry)
Fraxinus americana (White Ash)
Gymnocladus dioicus (Kentucky Coffee Tree)
Juniperus virginiana (Eastern Red Cedar)
Liriodendron tulipifera (Tulip Tree)
Magnolia acuminata (Cucumber Tree)
Morus rubra (Red Mulberry)
Prunus serotina (Black Cherry)
Sorbus americana (American mountain Ash)
Thuja occidentalis (Eastern White Cedar)
Tilia americana (Basswood)
Ulmus americana (American Elm)
Species Used in Appendix A-2 (n=15)
Abies balsamea (Balsam Fir)
Betula papyrifera (White/Paper Birch)
Fagus grandifolia (American Beech)
Larix laricina (Larch / Tamarack)
Picea glauca (White Spruce)
Picea mariana (Black Spruce)
Picea pungens (Blue Spruce)
Pinus banksiana (Jack Pine)
Pinus resinosa (Red Pine)
Pinus strobus (White Pine)
Quercus alba (White Oak)
Quercus macrocarpa (Bur Oak)
Quercus palustris (Pin Oak)
Quercus rubra (Red Oak)
Tsuga canadensis (Eastern Hemlock)
Species Used in Appendix A-3 (n=5)
Carya cordiformis (Bitternut hickory)
Carya ovata (Shagbark Hickory)
Juglans nigra (Black Walnut)
Populus grandidentata (Large‐Tooth Aspen)
Populus tremuloides (Trembling Aspen)
Akhmetzhanova AA, Soudzilovskaia NA, Onipchenko VG, Cornwell WK, Agafonov VA, Selivanov IA, Cornelissen JHC. 2012. A rediscovered treasure: Mycorrhizal intensity database for 3000 vascular plant species across the former soviet union. Ecology 93(3):689-90.
Allen MF. 1991. The ecology of mycorrhizae. New York: Cambridge University Press.
Bagyaraj J. 1991. Ecology of vesicular-arbuscular mycorrhizae. In: Handbook of applied mycology: Soil and plants. Arora DK, editor. New York: M. Dekker. 3 p.
Ecoregions of North America [Internet]. United States: US Department of Agriculture Forest Service; c2003 [cited 2013 . Available from: http://www.fs.fed.us/rm/ecoregions/products/map-ecoregions-north-america/# .
Chalot M and Plassard C. 2012. Ectomycorrhiza and nitrogen provision to the host tree. In: Ecological aspects of nitrogen metabolism in plants. Polacco JC and Todd CD, editors. Ames, Iowa: Wiley-Blackwell.
Dighton J. 2003. Fungi in ecosystem processes. New York: M. Dekker.
Eissenstat DM. 1992. Costs and benefits of constructing roots of small diameter. J Plant Nutr 15(6-7):763-82.
Harley JL and Harley EL. 1987. A check-list of mycorrhiza in the british flora. New Phytol 105(2, A Check-List of Mycorrhiza in the British Flora):1-102.
Hempel S, Gatzenberger L, Kahn I, Michalski SG, Rillig MC, Zobel M, Moora M. 2013. Mycorrhizas in the central european flora: Relationships with plant life history traits and ecology. Ecology 94(6):1389-99.
Smith SE and Reid DJ. 2008. Growth and carbon economy of arbuscular mycorrhizal symbionts. In: Mycorrhizal symbiosis. Smith SE and Reid DJ, editors. 3rd ed. ed. Boston: Elsevier/Academic Press. 117 p.
Trappe JM. 1987. Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Ecophysiology of VA mycorrhizal plants. Safir GR, editor. Boca Raton, Fla.: CRC Press. 5 p.
Digital representation of “Atlas of United States Trees” by Elbert L. Little, Jr. [Internet]. United States: US Geological Survey; c1999 [cited 2013 . Available from: http://gec.cr.usgs.gov/data/little .
Wang B and Qiu Y-. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299-363.