Abundance of root clusters in Kingia australis (Dasypogonaceae) highlights widespread non-symbiotic adaptations to nutrient-impoverished soils

doi:10.21203/rs.3.rs-5090992/v1

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Abundance of root clusters in Kingia australis (Dasypogonaceae) highlights widespread non-symbiotic adaptations to nutrient-impoverished soils

https://doi.org/10.21203/rs.3.rs-5090992/v1

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Background and Aims: Recent erosion of a riverbank in southwestern Australia exposed previously unrecorded root clusters produced by the grasstree, Kingia australis (Dasypogonaceae). Our aim was to provide descriptions of these structures compared with currently known specialized roots.

Methods: Excavation of root clusters, quantification of their distribution/morphology, and histology.

Results: There were 260 clusters per m³ of soil to a depth of 1.6 m and concentrated at 50-70 cm. They averaged 8.4 x 5.5 cm in length x width with 5360 roots/rootlets per L of rhizosphere soil. Clusters comprised a parent lateral (with cortical aerenchyma), secondary parent roots 50 x 3 mm in length x width, and rootlets 10 x 1 mm. Clusters are perennial, new roots sometimes emerging from the previous winter-growing-season’ cluster. We refer to these novel structures as staghorn-coralloid roots. Total root length reached 70 m per L of soil. The epidermal surface averaged 1600 cm² per L of soil. All roots are covered in root hairs, with parent lateral hairs 250 µm long to 700 µm for rootlets. They must push through a ±150-µm thick mucigel layer to reach the soil. Adding root hairs increased the surface area exposed to the rhizosphere by 4.4 times for a mere 3.3% increase in root volume. Endogenous fungal hyphae or (cyano)bacteria were not evident.

Conclusion: These root clusters link with proteoid, dauciform and capillaroid roots via their prolific production of extremely hairy rootlets with abundant mucigel, implying that they are functionally matched, but are otherwise morphologically and anatomically distinct.

Dasypogon

Kingia

mucigel

phosphorus

oligotrophic soils

root clusters

root hairs

root surface area

The floras of landscapes with a long history of recurrent fire, nutrient-impoverished soils, prolonged seasonal drought and/or waterlogging, and intense herbivory/granivory, are surprisingly species rich. It is clear that environmental stresses and disturbances serve to promote species co-occurrence and speciation (Allsopp et al. 2014, Groom and Lamont 2015, He et al 2019, Brundrett 2021). These trends fit the right-hand side of the classic hump-shaped response curve, with species richness increasing as the environmental variable becomes less favourable for growth and reproduction (Lamont 2024). This is illustrated in Fig. 1, where the number of species with proteoid root clusters and mycorrhizas quadrupled as total P per unit soil weight halved in the well-documented, nutrient-impoverished soils of sclerophyll shrublands in southwestern Australia (Lambers et al. 2013, Lamont and Keith 2017).

There is possibly no better example of this environmental relationship than the grasstree, Kingia australis (Dasypogonaceae). The family separated from the palms (Arecaceae) > 125 million years ago (Ma) but Kingia itself originated < 34 Ma (Givnish et al. 2018); i.e., as the Earth changed markedly from overall hot, humid climates in the Oligocene to increasingly a) cool, dry and seasonal climates, b) seasonally fireprone, and with c) carbon-dioxide-limited photosynthesis, through the Miocene (Osborne 2008). Kingia became so adaptively distinct that there has even been an attempt to place it in its own family (Kingiaceae Schnizlein). This species (monotypic genus, tribe, subfamily) is endemic to fireprone sclerophyll shrublands (such as those cited in Fig. 1) to open eucalypt forests in southwestern Australia (Fig. 2A). The climate is hot to warm mediterranean with 350−1,000 mm of rain per annum (prior to recent global warming) mostly falling in winter-spring, with summer drought lasting 4−6 months and temperatures often exceeding 45°C, but frosts are rare. Soils vary from quartzitic sand over a shallow claypan in seasonally waterlogged lowlands to massive laterite over kaolinitic clay in uplands with available P often < 10 mg kg^− 1 soil (McArthur 1991). The long needle leaves, rhombic in transection, are highly sclerified with sunken stomata (xeromorphic) and, while strongly herbivore-resistant, are highly flammable. Flowering is stimulated by fire. Pollination is by both insects and birds (e.g., Lichmera indistincta, pers. observ.) that alight on the terminal ‘crown’ of drumstick-shaped inflorescences, and no doubt their droppings add to the value of the leafbases as a source of nutrients for the embedded ‘prop’ roots (see below). Ripe seeds are released explosively from the capsules.

Kingias produce floral primordia every year but prolific flowering is dependent on incineration of the crown (Lamont and Downes 1979). The persistent leaves are burnt back to their fire-resistant mantle of leaf bases. Highly lignified, primary aerial roots arise from near the apex and push their way through the mantle, up to 3,000 reaching the soil of a 6-m tall plant, taking an estimated 35 years to do so (Lamont 1981a). These act as concealed prop roots obviating the need for anomalous secondary growth that characterizes palms and other grasstrees, such as Xanthorrhoea. Laterals branch out into the leafbases where they are effective in uptake of water and (labelled) phosphate, HPO₄⁻ (Lamont 1981b). This work has shown that, on a volume basis, the leaf bases are a better source of water and nutrients that the sandy soil in which the plant resides. Kingias often grow in winter/spring-waterlogged soils and the abundant cortical aerenchyma in the primary roots no doubt serves to supply oxygen to roots penetrating these soils. The stem pith has remarkable longevity, a well-defined ‘deathfront’ separating the living tissue, recorded up to an age of 435 years, from the dead tissue beneath (Lamont 1980). Clearly, this unique combination of traits has enabled Kingias to adapt effectively to the special constraints of this highly fire/drought-prone, severely nutrient-impoverished and efficient herbivore-exposed region. Providing just a single contribution to species diversity, Kingias make a unique and significant contribution to the world-renowned biodiversity of this region (Groom and Lamont 2015, Brundrett 2021).

Recently, we became aware that some of the special features of Kingias even existed belowground. One of us (AW) was hiking along the dry bed of the Sabina River located 230 km south of Perth in SW Australia, when many clumps of roots were observed protruding from the eroded banks (Fig. 2B). The laterals supporting the clumps could be traced back to Kingias abutting the banks. Inspection of photos convinced one of us (BL) that they were a type of root cluster previously unrecorded. A project was therefore instigated to examine these structures in more detail with the aims to a) relate them to what is already known about the root system of Kingias, b) describe their morphology and anatomy, and c) compare them with known root-cluster types that possess abundant rootlets and root hairs with which they seemed most similar. Consideration was given to environmental factors that might stimulate their formation and their function to provide hypotheses for future experimental research.

Study site

The study was undertaken at an eroded bank face beside the Sabina River in the Whicher Range National Park in southwestern Australia (33.76955° S, 115.45860° E) (Fig. 2). Roots were examined in detail and sampled on 31 July 2024 following substantial rain in July (winter rain, May-July, was 394 mm) and the mean temperature range over that time was 4.3−25.6°C. The river began to flow on 27 July. The soil was lateritized silt-clay-loam (sand was fine) grading to pisolitic laterite in silt-clay at 1.8 m with massive laterite at 2.0 m (over which the river flows). Soil colour was noted at 10 cm intervals down the profile (Munsell Soil-Color Charts, 2009). The pH (slurry with 1:1 rainwater at pH 6.8 with calibrated pH meter) of the kaolinitic clay-loam surrounding four root clusters was 6.0−6.4.

The vegetation is eucalypt woodland, 6−8 m tall (Corymbia calophylla, Eucalyptus marginata), with scattered shrubs, 2−3 m tall (Grevillea manglesioides, Hakea lasianthoides), and grasstrees (Xanthorrhoea preissii, Kingia australis, Dasypogon hookerii), 1−5 m tall, and a species-rich, small-shrub−perennial-herb layer (Proteaceae, Myrtaceae, Fabaceae, Cyperaceae, Restionceae). Five Kingias were located within 1 m of the breakaway face at the study site (Fig. 2A) and the cluster parent laterals were traced to the base of several of these (also see Lamont 1980a for a description of the root system of this species).

Root cluster analyses

Counts were made of the numbers of root clusters evident at 10-cm intervals down the profile for three contiguous 1 x 1.8 m profiles for the most accessible face where clusters were prominent. Assuming that 25 cm of the profile face had been eroded away (by restoring the horizontal position of pendulous clusters as evidence), the data were converted to per soil volume (equivalent to cluster volume). Photographs of the profile were taken, with and without a ruler for scale, and the images used to estimate the length and width of 50 clusters.

Three current season’s clusters were located embedded in the profile, excavated and taken in plastic bags to the ‘laboratory’ (Helen Duff’s dining room) for quantitative assessment. Older clusters were also harvested for comparative purposes. Rhizosphere soil was brushed away from each of the three new-season clusters for later determination of Munsell colour and pH. They were dunked repeatedly in rainwater until all loose soil was removed. Their three dimensions were then measured with vernier callipers (all values were to 0.1 mm and occasionally to 0.05 mm as required). They were photographed in colour under a frosted, GLS, LED 9-W light source with an iPhone 12 (Apple), double-lens camera with 15.6.1 software. They were then separated into primary parent root, secondary parent roots and rootlets, their number counted, and the lengths and widths of 30 representative rootlets per cluster, and all of the other roots (1 to 24 in number or 30 if more than 30 present), measured with callipers. A few roots were selected for microscopy. The three batches of root types were placed on paper towelling, patted dry and their wet weights taken to 0.01 g.

Mathematical formulae were then used to determine number of roots per unit volume of soil within the confines of the clusters, total root lengths per unit volume of soil, root volume (LπD³/6), and root surface area (LπD) where L = total length and D = diameter. Root hair values were obtained from Lamont (1981a) as we were not able to acquire sufficiently accurate details here.

Anatomy

Fresh, representative roots were placed longitudinally between carrot tuber segments and transections, ~ 0.3 mm wide, obtained with a safety razor blade. They were placed on glass slides and stained with 1% aqueous brilliant blue, cover slip added and viewed under a dissecting microscope for checking quality. For estimation of root-hair length, sections were placed directly on slides with a ruler in mm. Five representative root hairs for each of five roots, or different parts of the same root if numbers were insufficient, were measured. Suitable slides were placed under a transmission microscope with camera attachment (Omax, model A3RDF50, China) and images captured with an iPhone 14 Promax. Scales for the images were estimated from known dimensions of the roots. Images were used to count number and width of root hairs. To show the presence of aerenchyma confined to the parent roots, a cross-section specimen was critical-point dried and photographed with a scanning electron microscope (Lamont 1983b).

Density was estimated from hairs per unit length of root perimeter x section width. These were converted to root-hair volume and area per unit root-surface area using the mean root-hair length per root type (Table 1) and the above formulae. Total root-hair volume and area per L of soil were estimated from mean volumes and surface areas per root type (Table 1). It should be noted that accurate values for all root-hair measurements would require detailed studies of wax-embedded specimens so that the estimates for root-hair properties must be regarded as indicative rather than definitive, but the trends are clear.

Soil profile distribution

Soil colour was in the range yellow-red with black humus dominating colour in the uppermost 20 cm (A1 horizon) becoming brown at a depth of 60-80 cm and orange from 110 cm (Fig. 3, also see Fig. 2A). 50 root clusters varied in length from 8 to 28 cm and width from 4 to 15 cm, with a mean ± 95% confidence interval of 15.2 ± 2.0 x 10.0 ± 2.0 cm. Clusters were rare in the A horizon, peaking in the B horizon at 50-70 cm, averaging almost 500 clusters per m³ of soil in that section, and declining (as with the supporting laterals) to zero by 170 cm. This gives a mean of 260 clusters per m³ in the uppermost 150 cm of soil. Elsewhere we noted that where the soil was deeper some clusters occurred at a maximum depth of 200 cm. Thus, their distribution formed a highly significant quadratic curve (Fig. 3).

Cluster morphology

There was minor variation in cluster volume and wet weight among the three analysed in detail, averaging 107 mL and 20 g (Table 1). Wet weight averaged 230 g per L of cluster. Sometimes clusters were aggregated into 3-4 clumps, possibly representing different seasons as well, making identification of individual clusters difficult. The finer the root type the more it contributed to mass, with rootlets averaging 50% total weight and secondary parent roots 37%. The primary parent root varied greatly in its (small) contribution to mass as care was not taken to ensure these were always within the confines of the cluster. Secondary root abundance was 20x that of the primary, and rootlets were 24x more abundant than the secondary roots, with rootlets accounting for 96% of the total number on average, and 5140 rootlets per L of soil within the confines of the cluster (Table1). Fig. 4 shows the trends graphically.

Table 1. Dimensions of three root clusters, with their means, collected from the Sabina River study site 31 July 2024. Soil/cluster refers to rhizosphere soil located within the confines of the cluster. Munsell colours of rhizosphere soils have been added to column headings.

Root length within the secondary and rootlet categories varied greatly as they were actively growing at the collection time and producing new roots (Table 1). Secondary roots (47 mm) averaged four times the length of rootlets (11 mm). Rootlets accounted for 84% of total root length with a mean of 57 m per L of soil/cluster. Root diameter was less variable within each category with the primary root averaging twice that of the secondary (2.9 mm) that in turn was twice that of the rootlets (1.2 mm). Combining these gave rootlets accounting for 43.5% of root volume occupying 16% of the soil volume within the confines of the cluster, but 67% of total root surface area, equivalent to an area of 40.5 x 40.5 cm² per L of cluster/rhizosphere soil.

Microscopy

The three root categories recognized here have a typical monocotyledonous anatomy with a well-defined stele and cortex with a dense cover of medium-sized root hairs (Fig. 5B, D). Root hair length varied from 0.1 to 1.1 mm (Table 1). The hairs of rootlets averaged 54% longer (0.7 mm) than for the secondary roots (0.5 mm) and 270% longer (0.26 mm) than for the primary roots. Widths vary from a mean of 12.5 µm for primary laterals to13.6 µm for secondary and rootlets (from Lamont 1981a). Density averages 167 root hairs per mm² of root surface. Combining these data gives rootlets contributing 60% of root hair volume while adding just 3.3% to the volume of the cluster plus associated soil (Table 1). Root hairs add 7150 cm²per L^-1 soil/cluster, increasing the total area exposed to the soil by 4.36 times, with rootlets accounting for 77% of this increase.

The parent laterals possess large, radially-aligned, schizogynous airspaces in the cortex (aerenchyma) that make the root spongy to the touch (Fig. 5D). The root hairs are sometimes crowded onto micro-mounds of 30 or more hairs that produce pincushion-like structures resulting in hairs from adjacent mounds interweaving with slight depressions in between. This adds to the root sponginess and appears to facilitate water retention. The daughter roots lack this interwoven structure of the hairs as there are no mounds. They also lack aerenchyma, consisting entirely of standard parenchyma cells (Fig. 5A). Since the sections were not washed and relatively thick, any hyphae or (cyano)bacteria should have been visible in the cortex but none was evident. A prominent mucigel layer, 100-200 µm thick, surrounded the secondary roots and rootlets (Fig. 5). This layer stained darkly with brilliant blue. Root hairs need to push through this mucigel layer to reach the soil. Colloids, apparently iron-oxide impregnated associated with the lateritic soil, sometimes forming microlumps, were present in the mucigel that appeared to give the roots their orange appearance (Fig. 2). Humic and clay particles and tiny silica grains were also embedded among the mucigel. Daughter roots/rootlets arose randomly from the pericycle of the parent root.

The discovery of abundant clusters of roots through the soil profile in a grove of Kingia australis shows that the occasional clumps of lateral roots previously reported on the caudexes of this species (Fig. 5D, Lamont 1981a) are, in fact, far more abundant in the soil. They are now shown to be discrete root clusters, an order of magnitude larger than the other three root-cluster types currently recognized, other than compound proteoid roots (Table 2). They terminate lateral roots ultimately arising from the primary prop roots embedded in the persistent leafbases of this grasstree. In describing their appearance, comparison with staghorn coral is obvious (Fig. 2). The term ‘coralloid’ has already been pre-empted by the root clusters of cycads, although it is less apt as the rootlets of coralloid roots bifurcate (Lamont 1982) that real coral does not. We therefore propose that they be called staghorn-coralloid roots.

The absence of longitudinal rows of rootlets distinguishes these root clusters from proteoid roots. There is no basal swelling of the rootlets as in dauciform roots. They do not form a soil-surface mat as in capillaroid roots. Having two sizes of root division is also unique, although sometimes daughter proteoid root may arise within the confines of a parent proteoid root (Lamont 1983a). At an average width of 2.9 mm (secondary parent) and 1.2 mm (rootlets), the roots are coarser than other root-cluster types. What groups them are a) their discrete morphology located along otherwise bare laterals, b) presence of crowded rootlets, c) presence of a dense cover of root hairs, and c) lack of endogenous microbial symbionts. Table 2 makes it clear that similar, non-symbiotic clusters of roots densely covered in root hairs are widespread throughout the world’s nutrient-impoverished soils, especially if they are also waterlogged as is the case with some habitats of Kingia.

These root clusters support the emerging rule that, as roots become thinner, they become hairier, individually shorter, their length per unit total root mass increases (by definition), and their surface area rises exponentially with almost negligible increase in root volume or mass (Table 1, Fig. 5). Contact with the rhizosphere increases markedly and can be expected to enhance root function on three fronts: a) exudation of organic and phenolic acids, sugar derivatives, and enzymes, b) enhanced activity of beneficial microbes, and c) absorption of water and nutrients mobilized by these processes (Lamont 2003, Lambers et al. 2006). Even so, the rootlets of staghorn-coralloid roots are not as fine as those listed in Table 2 and it is therefore doubtful that they are as metabolically efficient. Nevertheless, their unique features and location in the soil profile may give them adaptive advantages yet to be explored.

The abundance of root clusters in wetlands (sedges, restios, Viminaria, Hakea sulcata) needs further consideration, and may reflect the unsuitable conditions for symbiotic microbes in waterlogged soils and/or ease with which root hairs can form at the soil surface. Lamont (1976) showed how proteoid root production of Hakeas is enhanced in waterlogged soils (low redox potential) despite severe reduction in growth of the rest of the root system. That Kingia has a waterlogged ancestry is indicated by the abundance of aerenchyma in the primary prop roots (Fig. 5D), even among upland plants, only ceasing on reaching the root clusters.

It is intriguing that staghorn-coralloid roots are not preferentially located in the high-humus part of the soil profile as with other root-cluster types (Lamont 2003) but peak at a depth of 50-70 cm (Fig. 3). This is consistent with the lateral spread of parent roots through the profile of this species (Lamont 1981a). So, the prior question might be why do the parent roots concentrate in this region? First the primary roots have a direct downward path as they emerge from the caudex from which they later spread and then they stop production as they near the water table or bedrock, as here. Second, they may not need a microbial stimulus to promote their initiation, unlike proteoid roots (Lamont et al. 2015), or root nodules or mycorrhizas, that obliges these roots to form in the microbially-rich humus layers.

Third, the B horizon may be almost as good, or a better, source of exchangeable nutrients, such as P or K, in these highly leached soils than the A horizon (see Table 3 in Lamont 2003 for support). Pate et al. (2001) showed how organic acids exuded by proteoid roots chelate Fe and Al phosphates in the A horizon where they are carried to, and then deposited in, the B horizon. This is the reason why these lateritic soils are so orange in the B horizon, as are the embedded roots (Fig. 2). So, it is possible that this horizon is a rich source of insoluble nutrients that can be accessed by the well-established solubilizing powers of root clusters via organic acids and phosphatases (Lambers et al. 2006). The rhizosphere soil of current season roots averaged a pH of 6.2 compared with 6.7 around old roots, i.e., the rhizosphere of active roots is three times more acidic than moribund roots, giving support for this possibility. Earlier work showed that these clusters (undefined at the time) are highly efficient at absorbing P-labelled HPO4^2- injected between the leaf bases where it is translocated throughout the plant (Lamont 1981b).

Unlike proteoid and dauciform roots, but like root nodules, staghorn-coralloid roots appear to be not just terminal to the parent lateral but also perennial. That a new cluster may develop from within the previous season’s cluster is clear (Fig. 2E). Multiple clumps of rootlets cohering into a massive structure were sometimes observed. Whether the old rootlets remain metabolically active is unclear. Their root hairs whither and the mucigel-colloid mix turns a powdery grey (Fig. 2B). But these roots have been exposed to the air so that clusters not so exposed might remain functional. At this depth in the profile, the soil is more likely to remain moist throughout the year and adds to possible reasons for their preferential formation in the B horizon and explains their perenniality.

Acknowledgements

We thank the Department of Biodiversity, Conservation and Attractions in Western Australia for permission to collect specimens from the Whicher Range National Park, Richard Clark for field assistance, and Prof. Em. William Stock (Edith Cowan University) for comments on the manuscript.

This project was opportunistic and self-funded.

Competing Interests

We declare no competing interests.

Author Contributions

AW initiated this project, all authors participated in field and laboratory work, BBL undertook all literature reading, mathematical analyses, figure and table preparation, and wrote the first draft of the manuscript. All authors approved of the submitted manuscript.

Data Availability

All data used for analysis are given here (Table 1) or can be provided by BBL (Figs. 2, 3).

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Abundance of root clusters in Kingia australis (Dasypogonaceae) highlights widespread non-symbiotic adaptations to nutrient-impoverished soils

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Root cluster analyses

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