Specialized roots of Velloziaceae weather quartzite rock while mobilizing phosphorus using carboxylates

Abstract

Campos rupestres is an extremely phosphorus (P)‐impoverished rocky ecosystem in Brazil. Velloziaceae is an important plant family in this environment, and some species colonize exposed quartzite rock. However, we know virtually nothing about their root development and nutrient acquisition within the rock outcrops and their possible role in rock weathering and landscape formation. We tested the hypothesis that Velloziaceae dissolve P from the rock, enhancing rock weathering. The study was carried out with two Barbacenia species (Velloziaceae) that colonize quartzite rocks. We assessed the root specializations and exudates, and determined the mineralogical composition of the rocks. The quartzite rocks contained a low concentration of total P in a matrix composed predominantly of silica. Using transmission electron microscopy, we show root growth perpendicular to the rock‐bedding planes. A micro‐XRF set‐up at the XRF beamline of a synchrotron evidenced root‐associated rock dissolution. The investigated roots show novel morphological and physiological specializations, coined vellozioid roots, which are highly effective at P acquisition. These carboxylate‐releasing roots function like other specialized roots in nutrient‐depleted soils. The rocks represent a barrier for most species, but due to their chemical and physical actions inside the rocks, vellozioid roots play a pivotal role in rock weathering, contributing to shaping the campos rupestres landscapes. A plain language summary is available for this article.

Vellozioid roots allow for habitat specialization among rock‐ and soil‐dwelling Velloziaceae in campos rupestres

“…Although the studied areas are located within the Cerrado, the very distinct rock parent material provided opportunities for a very distinct flora (Colli‐Silva, Vasconcelos, & Pirani, ; Silveira et al, ). Campos rupestres are known for their high plant species diversity (Alves & Kolbek, ; Le Stradic, Buisson, & Fernandes, ), which is strongly related to substrate heterogeneity (Luz et al, ; Negreiros, Le Stradic, Fernandes, & Rennó, ; Teodoro et al, ). The rock parent material is extremely nutrient poor, leading to nutrient‐impoverished soils, with acidic pH, high aluminium (Al) concentrations and low magnesium (Mg) and calcium (Ca) concentrations (Benites et al, ).…”

“…The samples were immediately stored in 50% (v/v) ethanol. Prior to mycorrhizal assessment, all the roots were examined for the presence of long root hairs that formed rhizosheaths or vellozioid roots (Brown et al, ; Pang et al, ; Teodoro et al, ) with a stereomicroscope (Leica M80) and photographed with a Leica DFC295 3.0 MP digital camera with focus stacking using Leica Application Suite 3.8.0 (Leica). The presence of rhizosheaths was recorded, if the roots still had soil attached after shaking the roots in the vials and gently scrubbing with a paint brush (Buckley, ).…”

“…When P is severely limiting, as in campos rupestres , root specializations are more efficient than mycorrhizas (Raven et al, ). Dauciform roots, sand‐binding roots forming rhizosheaths (Abrahão, Costa, Lambers, et al, ; Abrahão, Lambers, Sawaya, Mazzafera, & Oliveira, ; Oliveira et al, ) and the recently described vellozioid roots (Teodoro et al, ) are prevalent in campos rupestres . Rhizosheaths are soil sheaths strongly bound to the roots, associated with long root hairs that increase root–soil contact and mucilage release (Brown, George, Neugebauer, & White, ; North & Nobel, ; Pang, Ryan, Siddique, & Simpson, ), which enhances the uptake of poorly mobile P (Brown et al, ; Kidd et al, ; McCully, ; Zhang et al, ).…”

“…Rhizosheaths are soil sheaths strongly bound to the roots, associated with long root hairs that increase root–soil contact and mucilage release (Brown, George, Neugebauer, & White, ; North & Nobel, ; Pang, Ryan, Siddique, & Simpson, ), which enhances the uptake of poorly mobile P (Brown et al, ; Kidd et al, ; McCully, ; Zhang et al, ). Vellozioid roots (Figure c) were described in rock‐dwelling Velloziaceae, which is an ubiquitous plant family in campos rupestres ; they are capable of dissolving the quartzite rocks, releasing strongly bound P through carboxylate release and contributing to biological weathering of rocks (Porder, ; Teodoro et al, ). These vellozioid roots are therefore expected to be more effective in rocks than in soils.…”

“…Because Velloziaceae grow both in soil (Figure d) and on rocks without any soil (Figure e) (Alcantara et al, ), they provide an excellent model for testing habitat specialization in campos rupestres . If the vellozioid roots were more carbon‐costly than rhizosheaths, they would only be an advantage for rock‐dwelling species, where investment in them would be rewarded through the acquisition of monazite‐bound P (Teodoro et al, ). We expect that due to the costs of habitat specialization of the vellozioid roots, species with these roots might be less abundant in soils.…”