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Background and Aims Initiation of cluster roots in white lupin (Lupinus albus) under phosphorus (P) deficiency requires auxin signalling, whereas flavonoids inhibit auxin transport. However, little information is available about the interactions between P deficiency and flavonoids in terms of cluster-root formation in white lupin. Methods Hydroponic and aeroponic systems were used to investigate the role of flavonoids in cluster-root formation, with or without 75 μm P supply. Key Results Phosphorus-deficiency-induced flavonoid accumulation in cluster roots depended on developmental stage, based on in situ determination of fluorescence of flavonoids and flavonoid concentration. LaCHS8, which codes for a chalcone synthase isoform, was highly expressed in cluster roots, and silencing LaCHS8 reduced flavonoid production and rootlet density. Exogenous flavonoids suppressed cluster-root formation. Tissue-specific distribution of flavonoids in roots was altered by P deficiency, suggesting that P deficiency induced flavonoid accumulation, thus fine-tuning the effect of flavonoids on cluster-root formation. Furthermore, naringenin inhibited expression of an auxin-responsive DR5:GUS marker, suggesting an interaction of flavonoids and auxin in regulating cluster-root formation. Conclusions Phosphorus deficiency triggered cluster-root formation through the regulation of flavonoid distribution, which fine-tuned an auxin response in the early stages of cluster-root development. These findings provide valuable insights into the mechanisms of cluster-root formation under P deficiency.

Background White lupin (Lupinus albus) is a leguminous crop with elite adaptive ability in phosphorus-deficient soil and used as a model plant for studying phosphorus (P) use. However, the genetic basis of its adaptation to low P (LP) remains unclear. ATPase binding cassette (ABC) transports G subfamily play a crucial role in the transportation of biological molecules across the membrane. To date, identification of this subfamily has been analyzed in some plants, but no systematic analysis of these transporters in phosphorus acquisition is available for white lupin. Results This study identified 66 ABCG gene family members in the white lupin genome using comprehensive approaches. Phylogenetic analysis of white lupin ABCG transporters revealed six subclades based on their counterparts in Arabidopsis, displaying distinct gene structure and motif distribution in each cluster. Influences of the whole genome duplication on the evolution of L.albABCGs were investigated in detail. Segmental duplications appear to be the major driving force for the expansion of ABCGs in white lupin. Analysis of the Ka/Ks ratios indicated that the paralogs of the L.albABCG subfamily members principally underwent purifying selection. However, it was found that L.albABCG29 was a result of both tandem and segmental duplications. Overexpression of L.albABCG29 in white lupin hairy root enhanced P accumulation in cluster root under LP and improved plant growth. Histochemical GUS staining indicated that L.albABCG29 expression increased under LP in white lupin roots. Further, overexpression of L.albABCG29 in rice significantly improved P use under combined soil drying and LP by improving root growth associated with increased rhizosheath formation. Conclusion Through systematic and comprehensive genome-wide bioinformatics analysis, including conserved domain, gene structures, chromosomal distribution, phylogenetic relationships, and gene duplication analysis, the L.albABCG subfamily was identified in white lupin, and L.albABCG29 characterized in detail. In summary, our results provide deep insight into the characterization of the L.albABCG subfamily and the role of L.albABCG29 in improving P use.

Secondary root emergence is a crucial trait that shapes the plant’s underground system. Virtually every developmental step of root primordium morphogenesis is controlled by auxin. However, how the hormone controls cell separation in primordium-overlaying tissues through wall loosening is poorly understood. Here, we took advantage of white lupin and its spectacular cluster root development to assess the contribution of auxin to this process. We show that auxin’s positive role on rootlet emergence is associated with an upregulation of cell wall pectin modifying and degrading genes. Downregulation of a pectinolytic enzyme gene expressed in cells surrounding the primordium resulted in delayed emergence. Pectins were demethylesterified in the emergence zone and auxin treatment further enhanced this effect. Additionally, we report specific rhamnogalacturonan-I modifications during cortical cell separation. In conclusion, we propose a model in which auxin has a dual role during rootlet emergence: Firstly, through active pectin demethylesterification and secondly by regulating the expression of cell wall remodeling enzymes.

Background and Aims Knowledge of plant resource acquisition strategies is crucial for understanding the mechanisms mediating the responses of ecosystems to external nitrogen (N) input. However, few studies have considered the joint effects of above-ground (light) and below-ground (nutrient) resource acquisition strategies in regulating plant species responses to N enrichment. Here, we quantified the effects of light and non-N nutrient acquisition capacities on species relative abundance in the case of extra N input. Methods Based on an N-manipulation experiment in a Tibetan alpine steppe, we determined the responses of species relative abundances and light and nutrient acquisition capacities to N enrichment for two species with different resource acquisition strategies (the taller Stipa purpurea, which is colonized by arbuscular mycorrhizal fungi, and the shorter Carex stenophylloides, which has cluster roots). Structural equation models were developed to explore the relative effects of light and nutrient acquisition on species relative abundance along the N addition gradient. Key Results We found that the relative abundance of taller S. purpurea increased with the improved light acquisition along the N addition gradient. In contrast, the shorter C. stenophylloides, with cluster roots, excelled in acquiring phosphorus (P) so as to elevate its leaf P concentration under N enrichment by producing large amounts of carboxylate exudates that mobilized moderately labile and recalcitrant soil P forms. The increased leaf P concentration of C. stenophylloides enhanced its light use efficiency and promoted its relative abundance even in the shade of taller competitors. Conclusions Our findings highlight that the combined effects of above-ground (light) and below-ground (nutrient) resources rather than light alone (the prevailing perspective) determine the responses of grassland community structure to N enrichment.

Gevuina avellana and Lomatia dentata are Proteaceae species from evergreen temperate forests, but only G. avellana can colonize nutrient deprived volcanic depositions. We hypothesized that under nutrient deprivation, G. avellana would present higher survival, physiological performance, and adjustment regarding cluster root (CR) formation and carboxylate exudation rate than L. dentata. We evaluated relative growth rate, maximal photosynthetic rate, photochemical performance, nitrogen (N) and phosphorus (P) leaf concentrations, specific leaf area, photosynthetic P and N use efficiency (PPUE and PNUE), CR formation and carboxylate exudation rate. Plants were grown in a greenhouse, using recent volcanic substrate and watered with different nutrient Hoagland (H) solutions: modified full Hoagland, without P, without N, or tap water. Both species showed high survival. G. avellana exhibited higher growth rates (RGR), and higher CR number and biomass allocation under nutrient deprivation, but lower carboxylate exudation rates than L. dentata. Malate, oxalate and succinate were detected in root exudates of G. avellana but only oxalate in L. dentata. However, PPUE and PNUE were higher in L. dentata than in G. avellana . Our hypothesis was not entirely accepted, CR formation was more “constitutive” in G. avellana, and composition of carboxylates was more diverse, with lower exudation rates than L. dentata. Moreover, L. dentata showed higher PNUE and PPUE, partly explained by thinner leaves. Different responses are related with edaphic conditions, where both species inhabit: more diverse to G. avellana and restricted to developed soils to L. dentata.

The low bioavailability of nutrients, especially nitrogen (N) and phosphorus (P), is one of the most limiting factors for crop production. In this study, under N- and P-free nutrient solution (-N-P), nodulating white lupin plants developed some nodules and analogous cluster root structures characterized by different morphological, physiological, and molecular responses than those observed upon single nutrient deficiency (strong acidification of external media, a better nutritional status than -N+P and +N-P plants). The multi-elemental analysis highlighted that the concentrations of nutrients in white lupin plants were mainly affected by P availability. Gene-expression analyses provided evidence of interconnections between N and P nutritional pathways that are active to promote N and P balance in plants. The root exudome was mainly characterized by N availability in nutrient solution, and, in particular, the absence of N and P in the nutrient solution triggered a high release of phenolic compounds, nucleosides monophosphate and saponines by roots. These morphological, physiological, and molecular responses result from a close interplay between N and P nutritional pathways. They contribute to the good development of nodulating white lupin plants when grown on N- and P-free media. This study provides evidence that limited N and P availability in the nutrient solution can promote white lupin-Bradyrhizobium symbiosis, which is favourable for the sustainability of legume production.

International audience; White lupin produces cluster roots in response to phosphorus deficiency. Along the cluster root, numerous short rootlets successively appear, creating a spatial and temporal gradient of developmental stages that constitutes a powerful biological model to study the dynamics of the structural and functional evolution of these organs. The present study proposes a fine histochemical, transcriptomic and functional analysis of the rootlet development from its emergence to its final length. Between these two stages, the tissue structures of the rootlets were observed, the course of transcript expressions for the genes differentially expressed was monitored and some physiological events linked to Pi nutrition were followed. A switch between (i) a growing phase, in which a normal apical meristem is present and (ii) a specialized phase for nutrition, in which the rootlet is completely differentiated, was highlighted. In the final stage of its determinate growth, the rootlet is an organ with a very active metabolism, especially for the solubilization and absorption of several nutrients. This work discusses how the transition between a growing to a determinate state in response to nutritional stresses is found in other species and underlines the fundamental dilemma of roots between soil exploration and soil exploitation.

Southern South American Proteaceae can occupy soils that are rich in total phosphorus (P) but poor in available P (for example volcanic soils) thanks to their cluster roots (CR), which mine soil P. However, some southern South American Proteaceae occur in a wide range of soil nutrition. We hypothesized that CR formation and function are more responsive to nutrient soil availability in the widely-distributed Embothrium coccineum than in the narrowly-distributed Orites myrtoidea, which exclusively occurs in recent volcanic depositions. Survival, growth rate, CR formation (number, biomass) and function (carboxylate exudation, phosphatase activity) were evaluated in seedlings of both species after five months of growth in either a volcanic or organic substrate. E. coccineum exhibited full survival in both substrates, but had significantly lower growth, higher CR formation, higher CR citrate and malate exudation, and higher phosphatase activity in the volcanic substrate. By contrast, O. myrtoidea had similar growth rate in both substrates but 73% lower survival and null CR formation in the organic compared to the volcanic substrate. Variation in soil nutrient availability caused variation in growth and CR formation and function in a southern South American Proteaceae species of wider distribution, but not in a narrowly-distributed counterpart.

Banksia attenuata is a resprouting species growing in deep sand, while B. sessilis is a fire-killed species occurring in shallow sand over laterite or limestone. We aimed to discover the ecophysiological basis for their different distributions by exploring their investment in deep non-cluster roots and shallow cluster roots, and their cluster-root functioning. Deep-pot (1 m), shallow-pot (400 mm), hydroponic experiments and phosphorus (P)-extraction experiment were carried out. Biomass allocation, cluster-root exudation, plant P and leaf manganese (Mn) concentrations were measured. Banksia attenuata allocated more biomass to deep roots and less biomass to cluster roots than B. sessilis did in deep pots. The two Banksias released similar carboxylates in all experiments, with similar carboxylate-exudation rates in hydroponics. The carboxylate amount per unit cluster root of B. sessilis grown in shallow pots was greater than that of B. attenuata, and B, sessilis acquired more P than B. attenuata did in limestone substrate. Greater investment in deep roots for water uptake accounts for the presence of B. attenuata in deep sand, and vice versa for the absence of B. sessilis. A larger investment in cluster roots, which released greater amounts of carboxylates, likely accounts for B. sessilis occurring over limestone. Trade-offs in investment and cluster-root functioning support the species’ distribution patterns and life histories. Leaf Mn concentration was a good proxy for the plant capacity to acquire P.

summary When Myrica cerifera was grown in a number of 1/1-strength Hoagland's solutions, each lacking one mineral nutrient, cluster roots formed only in solutions lacking phosphorus (P). In seedlings initially fertilized with various P concentrations, cluster root formation decreased with increasing P supply and was totally suppressed in solutions containing ≥ 1 mg P l−1. As total root weight did not vary significantly between P treatments, the proportion of the root system expressed as cluster roots or non-cluster roots varied with phosphorus supply. A similar response to increasing levels of foliar-applied P suggests that it may be internal P concentration in the plant that determines the initiation of cluster roots and not external P levels in the soil. Nitrogen, supplied as fixed dinitrogen or nitrate, did not have any effect on development of cluster roots and it appears that the capacity of actinorhizal plants to fix nitrogen by symbiotic association with a soil micro-organism is of no significance to cluster root formation. While abundant root hair development and extensive mycorrhizal mycelium distribution in the rhizosphere may represent more efficient morphological forms of improving plant P uptake, the significance of cluster roots in relation to P nutrition and the mechanisms involved in their development warrant further investigation.

Rhizoremediation potential of different wild plant species for total (aliphatic) petroleum hydrocarbon (TPH)-contaminated soils was investigated. Three-week-old seedlings of Acacia inaequilatera, Acacia pyrifolia, Acacia stellaticeps, Banksia seminuda, Chloris truncata, Hakea prostrata, Hardenbergia violacea, and Triodia wiseana were transplanted in a soil contaminated with diesel and engine oil as TPH at pollution levels of 4,370 (TPH1) and 7,500 (TPH2) mg kg−1, and an uncontaminated control (TPH0). After 150 days, the presence of TPH negatively affected the plant growth, but the growth inhibition effect varied between the plant species. Plant growth and associated root biomass influenced the activity of rhizo-microbiome. The presence of B. seminuda, C. truncata, and H. prostrata significantly increased the TPH removal rate (up to 30% compared to the unplanted treatment) due to the stimulation of rhizosphere microorganisms. No significant difference was observed between TPH1 and TPH2 regarding the plant tolerance and rhizoremediation potentials of the three plant species. The presence of TPH stimulated cluster root formation in B. seminuda and H. prostrata which was associated with enhanced TPH remediation of these two members of Proteaceae family. These results indicated that B. seminuda, C. truncata, and H. prostrata wild plant species could be suitable candidates for the rhizoremediation of TPH-contaminated soil. Refereed/Peer-reviewed

Indexación: Scopus. Aims: Embothrium coccineum is a pioneer tree that produces cluster roots (CR) induced by phosphorus (P) or nitrogen (N) deficiency, but the role which both N and P play in CR formation for different E. coccineum populations is still unknown. We hypothesized that in E. coccineum, N influences the CR formation response, primarily induced by P limitation. However, this response depends on local adaptations to their specific conditions of geographic origin. Methods: Seedlings from three contrasting edaphoclimatic conditions (Northern, Central and Southern populations) were grown in hydroponic culture under high and low N supply and at five different P supply. Morphophysiological responses, including CR number, growth, biomass, P and N plant concentration, were studied. Results: Our results showed that at high N supply, CR formation was stimulated with increased P supply, but just until it reaches a maximum of 5 μM, above this concentration CR formation decreases. However, at low N supply, a constitutive response was observed regardless of P supply. Moreover, each of these responses depends on the populations. Conclusions: Our study suggests that N drives CR formation induced by P supply and that a differential response exists among E. coccineum populations, that could be related to their origin edaphoclimatic conditions. © 2020, Springer Nature Switzerland AG. https://link-springer-com.recursosbiblioteca.unab.cl/article/10.1007%2Fs11104-020-04622-0

Tissues of the Australian native plant species Hakea actities (Proteaceae) contain numerous metabolites and structural compounds that hinder the isolation of nucleic acids. Separate RNA and genomic DNA extraction procedures were developed to isolate high quality nucleic acids from H. actities. Total RNA was extracted from leaves, roots and cluster roots of H. actities grown in low nutrient levels. Cluster root formation in H. actities only occurs when the plants are grown in low nutrient concentrations. However, under these conditions, nucleic acid extraction becomes increasingly difficult. The new procedures are faster than many of the published nucleic acid extraction protocols, and avoid the use of hazardous chemicals. The RNA extraction method was used successfully on another Australian species and a crop species, suggesting that the procedure is useful for molecular studies of a broad range of plants.