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Mechanisms for enhancing nutrient uptake in plants, with particular reference to mediterranean South Africa and Western Australia

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Abstract

The major constraints to nutrient uptake by vascular plants in mediterranean South Africa and Western Australia are: very infertile soils, relatively low temperatures when water availability is high, and hot, dry summers. These constraints are partly overcome through increased efficiency of uptake, tapping novel sources of nutrients, and prolonging water uptake. Absorptive area per unit “cost” may be enlarged directly through increased fineness of the root system and proliferation of long root hairs. This reaches its greatest development in the root clusters of the Proteaceae (proteoid roots), Restionaceae (“capillaroid” roots) and Cyperaceae (dauciform roots). Absorptive area is increased indirectly through fungal hyphae which extend from hairless rootlets into the soil. Two major groups can be recognised: general (VA mycorrhizas) and host-specific (ericoid, orchid and sheathing mycorrhizas). Mycorrhizas are the most widespread specialised modes of nutrition and are probably universal in such major taxa here asPodocarpus, Acacia, Fabaceae, Poaceae, Asteraceae, Rutaceae, terrestrial orchids, Ericales and Myrtaceae. General mycorrhizas are the least drought-adapted of mechanisms for maximising absorptive area. All have been implicated in enhancing P uptake through increasing access to inorganic P, solubilisation and shortening the diffusion path. However, selective uptake of other nutrients, especially N, by host-specific mycorrhizas may be equally important.

Included under novel sources of nutrients are free N2 (utilised by N2-fixing nodules), small-animal prey (carnivorous leaves) and persistent leaf bases (aerial roots ofKingia australis). Both legume and non-legume N2-fixing species are well-represented in these two regions, with stands of individual species in southwestern Australia estimated to contribute 2–19 kg N/ha/yr to the ecosystem. Free nitrogen fixation requires additional nutrients, especially Mo and Co, but is enhanced following fires and by supplementary uptake mechanisms, especially VA mycorrhizas. Southwestern Australia is particularly rich in carnivorous species. Nitrogen, P, K and S are important nutrients absorbed, with digestion aided by enzymes provided by bacteria and the glands. Parasitic plants both tap novel sources of nutrients and capitalise on any efficient water and nutrient uptake mechanisms of the hosts. Root parasites are better represented than stem parasites in mediterranean South Africa and Western Australia. Phosphorus and K in particular are absorbed preferentially by the haustoria, but much remains to be known about their modes of operation.

Maximum activity of all uptake mechanisms, except those attached to some deep-rooted plants, is restricted to winter-spring. Most new seasons’s rootlets and specialised roots are confined to the uppermost 15 cm of soil, especially in or near the decomposing litter zone. Nutrient uptake is further enhanced by the tendency for the rootlets to cluster, trapping water by capillary action and prolonging nutrient release. As an early product of decomposition, N tends to be available as NH4 (rather than NO3) and it is absorbed preferentially by almost all specialised modes of nutrition. Microorganisms are required in the formation and/or functioning of all these structures, except haustoria. Uptake mechanisms which are optional to the plant reach their peak contribution to the root system at soil nutrient levels well below those required for greatest plant growth, when they may be absent altogether. It is only over the narrow range of nutrient availability, where shoot content of a nutrient is greater in the presence of the mechanism than in its absence (other factors remaining constant), that specialised modes can be termed nutrient-uptake “strategies.”

For all specialised modes of nutrition, the component genera are better represented in these two regions than in the surrounding more fertile, arid to subtropical regions of much greater area. Endemism of species with each mode exceeds that for the two floras overall (75%). This is taken as preliminary evidence that specialised modes of nutrition are best represented in nutrient-poor soils. While they serve to limit nutrient loss from the ecosystem, their proliferation is therefore not necessarily a response to increasing “leaks” in the system.

A hierarchical scheme of the functional/structural relationships between the various mechanisms is presented, starting with the rootless, VA-mycorrhizal plant as the most primitive condition. Taxa with many of the specialised modes of nutrition at present in southwestern South Africa and Western Australia have been evident in the pollen record since the early Tertiary Period. The absence of ectomycorrhizal forests in mediterranean South Africa, in marked contrast to Western Australia, can be traced to differences in their paleohistory. In both regions, the combination of fluctuating, but essentially diminishing, nutrient and water availability that began with the first mediterranean climate < 5 million years ago resulted in decimation of the less-tolerant rainforest ancestors on the one hand, and remarkable rates of speciation of the pre-adapted sclerophyll nucleus on the other.

Abstrakt

Die Haupthindernisse der Nährstoffaufnahme der Kormophyten des Mittelmeerklimas Südafrikas und Westaustraliens sind sehr nahrungsarme Böden, relativ niedrige Temperaturen, wenn genügend Bodenwasser zur Verfügung steht und heisse, trockene Sommer. Diese Hindernisse werden zum Teil durch erhöhte Leistungsfähigkeit von Nährstoffaufnahme, Anzapfung verborgener Quellen von Nährstoffen und Erhöhung und Verlängerung der Wasseraufnahme überwunden. Die Absorptionsfläche kann direkt durch die Feinheit des Wurzelsystems und die Entwicklung langer Wurzelhaare vergrössert werden. Diese Situation ist am besten durch die Wurzelbüschel der Familie Proteaceae (proteoid Wurzeln), die Kapillarwurzeln der Familie Restionaceae und die dauciform Wurzeln der Familie Cyperaceae repräsentiert. Indirekte Erhöhung der Absorptionsfläche ist durch Pilzfäden, die sich von haarlosen Wurzeln im Boden ausbreiten, gewährleistet. Hierbei können zwei Hauptgruppen beobachtet werden: allgemeine (VA Mykorrhizen) und wirt-spezifische (Ericales-, Orchideen- und Hüllmykorrhizen). Mykorrhizen sind die am weitesten verbreiteten, spezialisierten Arten erhöhter Nährstoffaufnahme und sind wahrscheinlich universal inPodocarpus, Acacia, Fabaceae, Poaceae, Asteraceae, Rutaceae, Land Orchideen, Ericales und Myrtaceae. Der Nährstoffaufnahmemechanismus der VA Mykorrhyzen ist der am wenigsten trockenresistente. Alle Mykorrhyzen haben die Fähigkeit entwickelt, grössere Mengen von Phosphor durch vergrösserten Zugang, erhöhte Auflösung und Verkürzung des Aufnahmeweges von inorganischem Phosphor aufzunehmen. Im Falle der wirt-spezifischen Mykorrhyzen ist jedoch bevorzugte Aufnahme anderer Nährstoffe, vor allem Stickstoff, gleichgalls wichtig.

Andere Quellen der Nährstoffaufnahme sind freier Stickstoff (ausgenutzt von N2-Bakterien in Wurzelknollen), Kleintierbeute in Blättern von Carnivoren und beharrende Blattbasen (Luftwurzeln vonKingia australis). Beide Formen von Legume- und Nichtlegume-Fixierung von N2 sind in diesen beiden Gegenden gut vertreten. In Südwestaustralien können einzelne Formen zwischen 2–19 kg N/ha/Jahr dem Ökosystem zuführen. N2-Fixierung benötigt zusätzliche Nährstoffe, vor allem Mo und Co. Es ist erhöht nach Busch (Wald) bränden und durch spezielle Ergänzungsaufnahme, vor allem in VA Mykorrhizen.

Südwestaustralien im besonderen ist reich an Carnivoren Spezies: N, P, K und S sind wichtige Nährstoffe, die aufgenommen werden. Die Verdauung von Kleintieren wird durch Enzyme bewerkstelligt, die von Bakterien und Drüsen ausgeschieden werden. Parasitische Pflanzen zapfen neue Quellen von Nährstoffen an und werten auch alle Vorrichtungen des Wirtes in Bezug auf erhöhte Wasser- und Nährstoffaufnahme aus. In den Mittelmeerklimaten Südafrikas und Westaustraliens sind Wurzelparasiten häufiger als Stammparasiten. Besonders P und K werden von den Haustorien bevorzugt aufgenommen, jedoch mehr Forschung ist nötig, um den Aufnahmemechanismus zu verstehen.

Mit der Ausnahme von tief-wurzelnden Pflanzen, optimale Nährstoffaufnahme ist auf die Winter-Frühlingszeit beschränkt. Dabei entwickeln sich Fein- und Spezialwurzeln innerhalb der oberen 15 cm-Bodenschicht, vorzugsweise innerhalb oder nahebei der Verwitterungszone des Laubes. Nährstoffaufnahme ist weiterhin durch Büschelformation der Feinwurzeln—wobei Wasser durch Kapillaraktion festgehalten und die Dauer der Nährstoffaufnahme verlängert wird—gesteigert. Ein zeitiges Produkt der Verwesung ist NH4, welches von bald allen spezialisierten Formen eher aufgenommen wird als NO3. Mit Ausnahme der Haustorien der Parasiten alle oben erwähnten Aufnahmeformen von Nährstoffen benötigen die Gegenwart von Mikroorganism. Nährstoffaufnahmemechanismen, die nicht unbedingt für die Pflanze notwendig sind, erreichen ihre grösste Verbreitung in der Bodenschicht, die weniger Nährstoffe enthält. In Bodenschichten mit einem hohen Nährstoffgehalt sind diese Mechanismen oft abwesend. In bezug auf die Verfügbarkeit von Nährstoffen ist es nur ein enger Bereich, in dem der Stengelnährstoffgehalt in der Gegenwart eines Spezialaufnahmemechanismus grösser ist als in der Abwesenheit eines solchen (wenn andere Faktoren gleich sind). In solchen Fällen kann man von Nährstoff aufnahme ‘Strategien’ sprechen.

Alle Spezialnährstoffaufnahmemechanismen sind in beiden Gegenden wohlvertreten. Dies steht im Gegensatz zu den umgebenden fruchtbareren ariden und subtropischen Gegenden. Endemismus von Spezies mit diesen spezialen Aufnahmeeinrichtungen übertrifft die anderen Spezies (75%). Diese Feststellung mag wohl zeigen, dass Spezialformen der Nährstoffaufnahme am besten in nährstoffarmen Böden gedeihen. Während diese dazu dienen, den Verlust von Nährstoffen vom Ökosystem zu vermindern, ist ihre Verbreitung innerhalb des Ökosystems nicht notwendigerweise eine Reaktion von zunehmenden ‘Lücken’ des Systems.

Ein Hierarchie-Schema der funktionalen/strukturalen Verwandtschaft der verschiedenen Mechanismen ist gegeben, beginnend mit der wurzellosen VA-mykorrhyzal Pflanze als die primitivste. Taxa mit vielen der verschiedenen Mechanismen der Nährstoffaufnahme sind in Südafrika und Westaustralien seit dem Früh-Tertiär—dokumentiert durch Pollenfunde—vertreten. Die Abwesenheit von ektotrophen Mykorrhyza Wäldern im Mittelmeerklima Südafrikas, im Gegensatz zu denen in Westaustralien, konnte durch die Verschiedenheit der Plaläohistorie erklärt werden. Die Kombination von Schwankungen, besonders der Abnahme der zur Verfügung stehenden Nährstoffe und des Wassers, die mit dem ersten Mittelmeerklima vor ungefähr 5 Million Jahren begann, resultierte in dem Verschwinden der weniger toleranten Regenwald Vorfahren auf der einen Seite und der Bemerkenswerten Fähigkeit zur Spezialisierung der Pro-sklerophyten auf der anderen Seite.

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Lamont, B. Mechanisms for enhancing nutrient uptake in plants, with particular reference to mediterranean South Africa and Western Australia. Bot. Rev 48, 597–689 (1982). https://doi.org/10.1007/BF02860714

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