Structure,ecology and physiology of root clusters – a review

Hairy rootlets, aggregated in longitudinal rows to form distinct clusters, are a major part of the root system in some species. These root clusters are almost universal (1600 species) in the family Proteaceae (proteoid roots), with fewer species in another seven families. There may be 10–1000 rootlets per cm length of parent root in 2–7 rows. Proteoid roots may increase the surface area by over 140× and soil volume explored by 300× that per length of an equivalent non-proteoid root. This greatly enhances exudation of carboxylates, phenolics and water, solubilisation of mineral and organic nutrients and uptake of inorganic nutrients, amino acids and water per unit root mass. Root cluster production peaks at soil nutrient levels (P, N, Fe) suboptimal for growth of the rest of the root system, and may cease when shoot mass peaks. As with other root types, root cluster production is controlled by the interplay between external and internal nutrient levels, and mediated by auxin and other hormones to which the process is particularly sensitive. Proteoid roots are concentrated in the humus-rich surface soil horizons, by 800× in Banksia scrub-heath. Compared with an equal mass of the B horizon, the A₁ horizon has much higher levels of N, P, K and Ca in soils where species with proteoid root clusters are prominent, and the concentration of root clusters in that region ensures that uptake is optimal where supply is maximal. Both proteoid and non-proteoid root growth are promoted wherever the humus-rich layer is located in the soil profile, with 4× more proteoid roots per root length in Hakea laurina. Proteoid root production near the soil surface is favoured among hakeas, even in uniform soil, but to a lesser extent, while addition of dilute N or P solutions in split-root system studies promotes non-proteoid, but inhibits proteoid, root production. Local or seasonal applications of water to hakeas initiate non-proteoid, then proteoid, root production, while waterlogging inhibits non-proteoid, but promotes proteoid, root production near the soil surface. A chemical stimulus, probably of bacterial origin, may be associated with root cluster initiation, but most experiments have alternative interpretations. It is possible that the bacterial component of soil pockets rich in organic matter, rather than their nutrient component, could be responsible for the proliferation of proteoid roots there, but much more research on root cluster microbiology is needed.     

Proteoid Root Development of Phosphorus Deficient Lupin is Mimicked by Auxin and Phosphonate

White lupin (Lupinus albus L.) develops proteoid (cluster) rootsin response to phosphorus deficiency. Proteoid roots are composedof tight clusters of rootlets that initiate from the pericycleopposite protoxylem poles and emerge from every protoxylem polewithin the proteoid root axis. Auxins are required for lateralroot development, but little is known of their role in proteoidroot formation. Proteoid root numbers were dramatically increasedin P-sufficient (+P) plants by application of the syntheticauxin, naphthalene acetic acid (NAA), to leaves, and were reducedin P-deficient (-P) plants by the presence of auxin transportinhibitors [2,3,5-triiodobenzoic acid (TIBA) and naphthylphthalamicacid (NPA)]. While ethylene concentrations in the root zonewere 1.5-fold higher in -P plants, there was no effect on proteoidroot numbers of the ethylene inhibitors aminoethoxyvinvylglycine(AVG) and silver thiosulphate. Phosphonate, which interfereswith plant perception of internal P concentration, dramaticallyincreased the number of proteoid root segments in +P plants.Activities of phosphoenolpyruvate carboxylase (PEPC), malatedehydrogenase (MDH) and exuded acid phosphatase in proteoidroot segments were not different from +P controls when NAA wasapplied to +P lupin plants, but increased to levels comparableto -P plants in the phosphonate treatment. Addition of TIBAor NPA to -P plants reduced PEPC and MDH activity of -P proteoidroots to levels found in +P or -P normal root tissues, but didnot affect acid phosphatase in root exudates. These resultssuggest that auxin transport from the shoot plays a role inthe formation of proteoid roots during P deficiency. Auxin-stimulatedproteoid root formation is necessary, but not sufficient, tosignal the up-regulation of PEPC and MDH in proteoid root segments.In contrast, phosphonate applied to P-sufficient white lupinelicits the full suite of coordinated responses to P deficiencyCopyright2000 Annals of Botany Company Lupinus albus L., white lupin, proteoid roots, auxin, ethylene, phosphonate, phosphorus deficiency     

Iron and phosphorus fertilizations and the development of proteoid roots in macadamia (Macadamia integrifolia)

Proteoid roots are reportedly an adaptation to soils with either low phosphorus (P) or iron (Fe) or both. Since macadamia (Macadamia integrifolia, a member of the family Proteaceae) is an important crop in Hawaii, a factorial experiment with soil P levels of 0, 150, and 500 mg/kg and Fe levels of 0, 5, and 10 mg/kg was conducted to evaluate the effects of P and Fe fertilizations and possible Fe x P interactions on proteoid root development and macadamia growth. The soil was a highly weathered Oxisol having 0.015 mg P/L and 0.03 mg Fe/L in the soil solution in its unamended state. Proteoid roots were reduced in number and as a percentage of the total root mass at the highest levels of P and Fe. Phosphorus, however was a major controlling factor. Optimum dry matter associated with at least 10% proteoid roots, corresponding to a P concentration approximately of 0.035 mg/L in soil solution and 0.10% P in leaves. Total Fe in leaves or the amount of Fe applied was not a good predictor of plant growth. In contrast, chlorophyll content, a surrogate of biologically active Fe, was. Soil-solution ratio of Fe ^1/3/ P (molar basis) could be used to predict the response of macadamia growth to P and Fe fertilizations.     

Phosphorus sources and availability modify growth and distribution of root clusters and nodules of native Australian legumes

A variety of native Western Australian legumes produced root clusters in sand culture confirming field and published observations. In general, these legumes grew equally well when supplied with organic or inorganic sources of phosphorus. The nitrogen content of shoots and roots varied little among treatments for all species, however, phosphorus content was always greater in plants supplied with inositol‐P. The plasticity of root growth in response to localized placement of organic and inorganic sources of phosphorus was demonstrated using a simple ‘split root’ technique. Total root dry weight was, on average, more than doubled in P‐amended sand when compared with non‐amended sand. Root clusters tended to be produced in areas of relatively high phosphorus concentration and nodules in areas of low phosphorus concentration. Levels of phosphorus in lateral roots grown in P‐amended sand were significantly different from lateral roots grown in the corresponding non‐amended sand. Growth increases averaging 70% for white sand to over 100% for yellow sand indicated a large degree of ‘plasticity’ in roots under conditions of heterogeneous supply of phosphorus. Spatially exclusive development of organs for the acquisition of nutrients is discussed in relation to requirements for carbon in organ production and maintenance.     

Cluster Roots: A Curiosity in Context

Cluster roots are an adaptation for nutrient acquisition from nutrient-poor soils. They develop on root systems of a range of species belonging to a number of different families (e.g., Proteaceae, Casuarinaceae, Fabaceae and Myricaceae) and are also found on root systems of some crop species (e.g., albus, Macadamia integrifoliaandCucurbita pepo). Their morphology is variable but typically, large numbers of determinate branch roots develop over very short distances of main root axes. Root clusters are ephemeral, and continually replaced by extension of the main root axes. Carboxylates are released from cluster roots at very fast rates for only a few days during a brief developmental window termed an ‘exudative burst’. Most of the studies of cluster-root metabolism have been carried out using the crop plant L. albus, but results on native plants have provided important additional information on carbon metabolism and exudate composition. Cluster-root forming species are generally non-mycorrhizal, and rely upon their specialised roots for the acquisition of phosphorus and other scarcely available nutrients. Phosphorus is a key plant nutrient for altering cluster-root formation, but their formation is also influenced by N and Fe. The initiation and growth of cluster roots is enhanced when plants are grown at a very low phosphate supply (viz. ≤1 μM P), and cluster-root suppression occurs at relatively higher P supplies. An important feature of some Proteaceae is storage of phosphorus in stem tissues which is associated with the seasonality of cluster-root development and P uptake (winter) and shoot growth (summer), and also maintains low leaf [P]. Some species of Proteaceae develop symptoms of P toxicity at relatively low external P supply. Our findings with Hakea prostrata (Proteaceae) indicate that P-toxicity symptoms result after the capacity of tissues to store P is exceeded. P accumulation in H. prostrata is due to its strongly decreased capacity to down-regulate P uptake when the external P supply is supra-optimal. The present review investigates cluster-root functioning in (1) L.albus (white lupin), the model crop plant for cluster-root studies, and (2) native Proteaceae that have evolved in phosphate-impoverished environments.     

Phosphorus acquisition from soil by white lupin (Lupinus albus L.) and soybean (Glycine max L.), species with contrasting root development

White lupin and soybean have contrasting root morphologies: white lupin develops proteoid or cluster roots, roots with discreet clusters of short, determinate branch roots (rootlets) while soybean develops a more fibrous root system with evenly distributed, longer branch roots. Growth and P acquisition by white lupin and soybean were compared in a soil high in bound, total P, with or without additional inorganic P applied in solution. Additional P increased biomass by 25% and doubled total P in soybean. In contrast, white lupin did not respond to additional P in biomass or total P. However added P decreased cluster development on proteoid roots indicating that white lupin sensed the added P. The reduction in cluster weight per plant was exactly countered by an increase in dry weight of other roots. Soybean root development responded to P application, proliferating branch roots with active meristems in the upper portion of the soil profile where P was applied, and reducing root weight to plant weight by 13%. White lupin did not proliferate roots in response to P application. When P was not added to soil, soybean and lupin acquired similar P per unit root dry weight. However, white lupin accumulated 4.8 times more P per unit root length, suggesting that P acquisition in these plants involved other mechanisms such as the exudation of P solubilizing compounds. Soybean accessed P by developing more root length thus colonising more soil volume than white lupin and, therefore, was better able to take advantage of the added P. Pericycle and root tip meristem activities were critical to the differences in root development between white lupin and soybean, and therefore their responses to plant and soil P.     

Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply

Despite their difference in potential growth rate, the slow-growing Brachypodium pinnatum and the fast-growing Dactylis glomerata co-occur in many nutrient-poor calcareous grasslands. They are known to respond differently to increasing levels of N and P. An experiment was designed to measure which characteristics are affected by nutrient supply and contribute to the ecological performance of these species. Nutrient acquisition and root and shoot traits of these grasses were studied in a garden experiment with nine nutrient treatments in a factorial design of 3 N and 3 P levels each. D. glomerata was superior to B. pinnatum in nutrient acquisition and growth in all treatments. B. pinnatum was especially poor in P acquisition. Both species responded to increasing N supply and to a lesser extent to increasing P supply by decreasing their root length and increasing their leaf area per total plant weight. D. glomerata showed a higher plasticity. In most treatments, the root length ratio (RLR) and the leaf area ratio (LAR) were higher for D. glomerata. A factorization of these parameters into components expressing biomass allocation, form (root fineness or leaf thickness) and density (dry matter content) shows that the low density of the biomass of D. glomerata was the main cause for the higher RLR and LAR. The biomass allocation to the roots showed a considerable plasticity but did not differ between the species. B. pinnatum had the highest leaf weight ratio. Root fineness was highly plastic in D. glomerata, the difference with B. pinnatum being mainly due to the thick roots of D. glomerata at high nutrient supply. The leaf area/leaf fresh weight ratio did not show any plasticity and was slightly higher for B. pinnatum. It is concluded, that the low density of the biomass of D. glomerata is the pivotal trait responsible for its faster growth at all nutrient levels. It enables simultaneously a good nutrient acquisition capacity by the roots as well as a superior carbon acquisition by the leaves. The high biomass density of B. pinnatum will then result in a lower nutrient requirement due to a slower turnover, which in the long term is advantageous under nutrient-poor conditions.     

The occurrence of dauciform roots amongst Western Australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae)

* The incidence of species that develop specialised 'dauciform' lateral roots, which are hypothesised to be important for phosphorus (P) acquisition, is uncertain. We investigated their occurrence in Australian reed, rush and sedge species, grown at low P concentration in nutrient solution, and studied the response of Schoenus unispiculatus (Cyperaceae) to a range of P concentrations. * We assessed the fraction of root biomass invested in dauciform roots, their respiration and net P-uptake rate, and the P status of roots and leaves. * Dauciform-root development occurred only in particular genera of Cyperaceae when grown at low P supply. Increased P supply was associated with increased growth of S. unispiculatus and increased leaf [P]. Dauciform-root growth was reduced by increased P supply, and reduced P uptake co-occurred with the complete suppression of dauciform roots. * The P-induced suppression of dauciform roots in Cyperaceae is similar to that observed for proteoid roots in members of Proteaceae and Lupinus albus. The response of dauciform roots to altered P supply and their absence from root systems of some sedge species are discussed in terms of managed and natural systems.     

Phosphorus Stress-Induced Proteoid Roots Show Altered Metabolism in Lupinus albus

Proteoid roots develop in Lupinus albus L. in response to nutrient stress, especially P. Proteoid roots excrete citrate and thus increase the availability of P, Fe, and Mn in the rhizosphere. In an effort to understand citrate synthesis and organic acid metabolism in proteoid roots of lupin, we have evaluated in vitro enzyme activities of citrate synthase (CS), malate dehydrogenase (MDH), and phosphoenolpyruvate carboxylase (PEPC) in proteoid and normal roots of plants grown with or without P. Organic acid concentrations, respiration rates, and dark 14CO2-labeling patterns were also determined. The in vitro specific activities of CS, MDH, and PEPC and in vivo dark 14CO2 fixation were higher in proteoid roots compared to normal roots, particularly under P stress. Western blot analysis showed that PEPC enzyme protein was more highly expressed in -P proteoid roots compared to other tissues. The majority of the fixed 14C was found in organic acids, predominantly malate and citrate. A larger fraction of citrate was labeled in P- stressed proteoid roots compared to other root tissue. Respiration rates of proteoid roots were 31% less than those of normal roots. The data provide evidence for increased synthesis of citrate in proteoid roots compared to normal roots, particularly under P stress. A portion of the carbon for citrate synthesis is derived from nonautotrophic CO2 fixation via PEPC in proteoid roots.     

Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin

Release of large amounts of citric acid from specialized root clusters (proteoid roots) of phosphorus (P)-deficient white lupin (Lupinus albus L.) is an efficient strategy for chemical mobilization of sparingly available P sources in the rhizosphere. The present study demonstrates that increased accumulation and exudation of citric acid and a concomitant release of protons were predominantly restricted to mature root clusters in the later stages of P deficiency. Inhibition of citrate exudation by exogenous application of anion-channel blockers such as ethacrynic- and anthracene-9-carboxylic acids may indicate involvement of an anion channel. Phosphorus-deficiency-induced accumulation and subsequent exudation of citric acid seem to be a consequence of both increased biosynthesis and reduced metabolization of citric acid in the proteoid root tissue, indicated by increased in-vitro activity and enzyme protein levels of phosphoenolpyruvate carboxylase (EC 4.1.1.31), and reduced activity of aconitase (EC 4.2.1.3) and root respiration. Similar to citric acid, acid phosphatase, which is secreted by roots and involved in the mobilization of the organic soil P fraction, was released predominantly from proteoid roots of P-deficient plants. Also ³³Pi uptake per unit root fresh-weight was increased by approximately 50% in juvenile and mature proteoid root clusters compared to apical segments of non-proteoid roots. Kinetic studies revealed a K _m of 30.7 μM for Pi uptake of non-proteoid root apices in P-sufficient plants, versus K _m values of 8.5–8.6 μM for non-proteoid and juvenile proteoid roots under P-deficient conditions, suggesting the induction of a high-affinity Pi-uptake system. Obviously, P-deficiency-induced adaptations of white lupin, involved in P acquisition and mobilization of sparingly available P sources, are predominantly confined to proteoid roots, and moreover to distinct stages during proteoid root development. Received: 10 September 1998 / Accepted: 22 December 1998     

Root of edaphically controlled Proteaceae turnover on the Agulhas Plain, South Africa: phosphate uptake regulation and growth

The influence of phosphorus (P) availability on growth and P uptake was investigated in South African Proteaceae: (1) Protea compacta R.Br., endemic on severely nutrient-impoverished colluvial sands; (2) Protea obtusifolia Bueck ex Meissner; and (3) Leucadendron meridianum I. J. Williams, the latter both endemic on comparatively fertile limestone-derived soils. Plants were grown hydroponically in 1000 L tanks at 0.01, 0.1 or 1.0 microm P for 14 weeks. Biomass accumulation was influenced by P availability, doubling as [P] increased from 0.1 to 1.0 microm. Total biomass was greatest for P. compacta, but L. meridianum and P. obtusifolia had two to four times greater relative biomass accumulation at 0.1 and 1.0 microm [P]. Proteoid root clusters developed at both 0.01 and 0.1 microm[P], but were suppressed at 1.0 microm [P]; this was a 10-fold lower [P] than previously reported to inhibit cluster root formation. Rates of net P uptake at 5 microm P decreased in response to increased P availability from 0.01 to 1.0 microm P. Significant between-species differences in rates of P uptake and capacity to down-regulate P uptake were observed: P. compacta < P. obtusifolia < L. meridianum. The species responses are discussed in terms of adaptation to mosaics in soil P availability and the high beta diversity in the natural habitat.     

Auxin transport inhibitors act through ethylene to regulate dichotomous branching of lateral root meristems in pine

Many soil fungi colonize the roots of pines to form symbiotic organs known as ectomycorrhizas. Dichotomous branching of short lateral roots and the formation of coralloid organs are diagnostic of ectomycorrhizas in many pine species, although the regulation of these changes in root morphology is not well understood. We used axenic root cultures of six pine species to examine the role of auxin, cytokinin, ethylene and nutrients in the regulation of root architecture. Surprisingly, extensive dichotomous and coralloid branching of lateral roots occurred spontaneously in Pinus taeda , P. halepensis and P. muricata . In P. sylvestris , P. ponderosa and P. nigra , treatment with auxin transport inhibitors (ATIs), the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) or the ethylene-releasing compound 2-chloroethylphosphonic acid (CEPA or ethephon) induced extensive dichotomous branching and coralloid organ formation. Formation of both spontaneous and ATI-induced coralloid structures was blocked by treatment with an ethylene synthesis inhibitor L-α-(2-aminoethoxyvinyl)glycine; this inhibition was reversed by either ACC or CEPA. In addition, the induction of this unique morphogenetic pattern in pine root cultures was regulated by nutrient levels. The morphology and anatomical organization of the chemically induced dichotomous and coralloid structures, as well as the regulation of their formation by nutrient levels, show a striking similarity to those of ectomycorrhizas.     

New insights into leaf and fine‐root trait relationships: implications of resource acquisition among 23 xerophytic woody species

Functional traits of leaves and fine root vary broadly among different species, but little is known about how these interspecific variations are coordinated between the two organs. This study aims to determine the interspecific relationships between corresponding leaf and fine‐root traits to better understand plant strategies of resource acquisition. SLA (Specific leaf area), SRL (specific root length), mass‐based N (nitrogen) and P (phosphorus) concentrations of leaves and fine roots, root system, and plant sizes were measured in 23 woody species grown together in a common garden setting. SLA and SRL exhibited a strong negative relationship. There were no significant relationships between corresponding leaf and fine‐root nutrient concentrations. The interspecific variations in plant height and biomass were tightly correlated with root system size characteristics, including root depth and total root length. These results demonstrate a coordinated plant size‐dependent variation between shoots and roots, but for efficiency, plant resource acquisition appears to be uncoupled between the leaves and fine roots. The different patterns of leaf and fine‐root traits suggest different strategies for resource acquisition between the two organs. This provides insights into the linkage between above‐ and belowground subsystems in carbon and nutrient economy.     

Clustered root distribution in mature stands of <Emphasis Type="Italic">Fagus sylvatica</Emphasis> and <Emphasis Type="Italic">Picea abies</Emphasis>

Distribution of small roots (diameter between 2 mm and 5 mm) was studied in 19 pits with a total of 72 m² trench profile walls in pure stands of Fagus sylvatica and Picea abies. Root positions within the walls were marked and transformed into x-coordinates and y-coordinates. In a GIS-based evaluation, zones of potential influence around each root were calculated. The total potential influence produced isoline maps of relative root influence zones, thus indicating small root clustering. The questions studied were (1) whether there were marked clusters of small roots in the soil and (2) whether trees surrounding the pit (defined as tree density) correlate with the root abundance and distribution on the trench profile walls. Small roots of both species showed maximum abundance in the top 20 cm of the soil, where pronounced root clusters occurred next to areas with only low root accumulation. The area of root clusters did not differ significantly between the two stands. Weighted clumping, WC, calculated as a product of root class, and its area was used as an index of root clustering, which again did not differ between beech and spruce stands. However, evaluations on a single root level showed that beech achieved the same degree of clustering with lower number of roots. Regardless of soil properties related to root clusters, a significantly higher clustering acquired per root for beech than for spruce suggests beech to be more efficient in belowground acquisition of space. Because none of the parameters describing root clustering were correlated with tree density around the investigated soil profiles, clusters of small roots are inherently present within the tree stands.     

小麦与蚕豆间作体系根系形态与磷吸收的定量解析

豆科与禾本科作物间作能够改变作物根系生长,但不同施磷水平下间作-根系形态-磷吸收之间的关系尚未明确.本研究通过田间定位试验和根箱模拟试验,研究不同种植模式(小麦单作、蚕豆单作和小麦-蚕豆间作)和不同磷水平下小麦和蚕豆的产量、生物量、磷吸收及根系形态特征,分析探讨不同施磷条件下小麦-蚕豆间作对根系形态和磷吸收的影响.结果...     

Plant functional traits along environmental gradients in seasonally dry and fire‐prone ecosystem

Questions: How does the abundance and richness of plant assemblages with different functional (regeneration and nutrient acquisition) traits vary with fire regime, moisture availability and substrate fertility? What is the role of different functional traits in maintaining plant diversity under changing environmental conditions in seasonally dry and fire‐prone environments? Location: Southwest Western Australia. Methods: Plant species abundance and soil nutrients were determined at 16 forest sites with variable fire histories across an aridity gradient. All plant species were classified based on their functional traits as (1) perennial or annual, (2) ectomycorrhizal, arbuscular mycorrhizal, ericoid mycorrhizal, orchid mycorrhizal, proteoid or other non‐mycorrhizal, (3) resprouters or seeder, and (4) nitrogen fixer or non‐fixer. We used a multivariate (fourth‐corner) technique to simultaneously test the significance and direction of the relationship between each of these traits and fire frequency, fire interval length, aridity, and soil N, P and C fractions. Results: The functional response of the vegetation to fire regime was minor and restricted to annual species, which comprised only ～4% of taxa. Proteoid and ectomycorrhizal species dominated over species with arbuscular and orchid mycorrhizal roots, N‐fixers dominated over non‐fixers, and seeders dominated over resprouters when N fertility was low but organic labile P was high. Further, proteoid and ectomycorrhizal species richness increased with aridity, while arbuscular mycorrhizal species richness decreased. Conclusions: While the functional composition of southwest Australian vegetation is largely insensitive to changes in fire regime, nutrient acquisition and, to a lesser extent, regeneration traits provide mechanisms for the vegetation community to adjust to changes in resource availability. Thus, diversity responses to environmental change in seasonally dry and fire‐prone ecosystems are likely to be primarily mediated by the composition of nutrient acquisition traits in the vegetation community.     

Root structure and functioning for efficient acquisition of phosphorus: Matching morphological and physiological traits

BACKGROUND: Global phosphorus (P) reserves are being depleted, with half-depletion predicted to occur between 2040 and 2060. Most of the P applied in fertilizers may be sorbed by soil, and not be available for plants lacking specific adaptations. On the severely P-impoverished soils of south-western Australia and the Cape region in South Africa, non-mycorrhizal species exhibit highly effective adaptations to acquire P. A wide range of these non-mycorrhizal species, belonging to two monocotyledonous and eight dicotyledonous families, produce root clusters. Non-mycorrhizal species with root clusters appear to be particularly effective at accessing P when its availability is extremely low. SCOPE: There is a need to develop crops that are highly effective at acquiring inorganic P (Pi) from P-sorbing soils. Traits such as those found in non-mycorrhizal root-cluster-bearing species in Australia, South Africa and other P-impoverished environments are highly desirable for future crops. Root clusters combine a specialized structure with a specialized metabolism. Native species with such traits could be domesticated or crossed with existing crop species. An alternative approach would be to develop future crops with root clusters based on knowledge of the genes involved in development and functioning of root clusters. CONCLUSIONS: Root clusters offer enormous potential for future research of both a fundamental and a strategic nature. New discoveries of the development and functioning of root clusters in both monocotyledonous and dicotyledonous families are essential to produce new crops with superior P-acquisition traits.