Feature: Root of the matter

This feature appeared in the November/December 2009 issue of Australian Life Scientist. To subscribe to the magazine, go here.

“The general bright green colour of the brushwood and other plants, viewed from a distance, seemed to promise fertility. A single walk, however, was enough to dispel such an illusion; and he who thinks with me will never wish to walk again in so uninviting a country.”

A young Charles Darwin wrote these words in his diary in March 1836, after walking through the heathlands and woodlands around Western Australia’s King George Sound, where Albany stands today.

Professor Hans Lambers says Darwin may be excused for his bleak assessment of what he took to be a geologically young landscape, with an unremarkable flora. The young ship’s naturalist was homesick, seasick and at low ebb as HMS Beagle headed home after its epic five-year expedition mapping the coast of South America. In the 19th century, Darwin probably had no peer as an observer and interpreter of the natural world. He was right about WA’s sandy soils being infertile but, otherwise, his observations were way off beam.

Lambers, head of the School of Plant Biology at the University of Western Australia, will be a speaker at ComBio 2009, the annual conference of the Australian Society for Biochemistry and Molecular Biology, in Christchurch, December 8-12. He says Darwin did not realise the WA landscape was extremely ancient, and that its superficially drab vegetation harboured one of the world’s richest assemblages of flowering plants.

Had he had been there six months later, he would have witnessed one of the world’s most dazzling wildflower displays, and would surely have questioned how such extraordinary botanical riches could spring from such sterile soils. That question has also occupied Lambers since he arrived at the University of Western Australia in 1998 with a PhD in plant physiology. And to find the answer, he had to dig beneath the surface. Literally.

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Root of the matter

The majority of the world’s higher plants form symbiotic associations with soil-dwelling fungi. In such partnerships, called mycorrhizas, the fungus’ huge network of hyphal filaments serves as an extended root system for the plant, plumbing a much larger volume of soil for nutrients than the plant could exploit with its own roots. In return, the host plant rewards the fungi with energy-rich photosyntates. A minority of plants – about 18 per cent worldwide – eschew such intimacy and expense and go it alone on their own roots.

In WA, says Lambers, the more impoverished the soil, the higher the proportion on non-mycorrhizal species. Curiously, in the very soils where plants would be expected to be most dependent on mycorrhizas, only six per cent of species have them. Yet, paradoxically, the most nutrient-deficient soils in WA support the greatest diversity of plant species – Lambers says there is a “beautiful correlation”.

One reason for the exceptional diversity, he says is that when nutrients are so scarce, productivity is greatly reduced. “The entire system moves very slowly, so it takes a long time for one species to out-compete others. By the time one species has begun to establish an edge over its competitors, fire or short-term climatic fluctuations changes the game, and that species may end up at a disadvantage.”

Lambers says the WA flora – and Australian flora in general – have the world’s highest percentage of bird-pollinated species. “In contrast, there are hardly any bird-pollinated species in Europe,” he says. “I was really intrigued by the high proportion of non-mycorrhizal species when I came to WA,” Lambers said.

Among the abstainers, three families dominate. The Proteaceae, Cyperaceae and Restionaceae. Casuarinaceae and some Fabaceae are mycorrhizal, but also have specialised roots. All have independently evolved elaborate but very different root systems that allow them to prosper on impoverished soils.

Nearly all WA Proteaceae genera produce proteoid roots. Many members of the sedge family Cyperaceae have dauciform roots, in which the fine lateral roots progressively reduce in length, resulting in a carrot-like profile. Restionaceae produce feathery capillaroid roots, while the pea-flowered Fabaceae and Casuarinaceae produce root clusters, the generic term for all these specialised root systems.

The Proteaceae includes spectacular Australian endemics like Banksia, Grevillea, Hakea, Telopea and Isopogon, and southern Africa’s Protea, Leucospermum and Leucodendron, which grow on similarly nutrient-impoverished soils in that country’s mega-diverse fynbos heathland.

Lambers says there are marked differences in the structure of cluster roots across the Proteaceae, and in when they are produced. In Hakea and Grevillea and most other WA genera, fine lateral roots emerge from the main roots, forming an ellipse. The root structures of Banksia are unique, and more complex, with the lateral roots producing secondary lateral roots of their own.

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Phosphate surprise

The WA hakea H. prostrata stops making cluster roots after accumulating enough phosphate in its leaves. However, the plant harboured a mystery that intrigued Lambers: unlike most other plants, it keeps taking up more phosphate when more phosphate is added to soil. This makes it extremely susceptible to phosphate toxicity, more so than most species, which down-regulate their phosphate uptake system when supplied with more of the chemical.

“The penny finally dropped about what these plants are doing,” says Lambers. “Mycorrhiza-forming species are scavengers that can exploit soluble nutrients beyond reach of the plant’s root system. Species with root clusters are specially adapted to mine phosphate. In WA’s most nutrient-depleted soils, mycorrhizas don’t work, because there is almost no soluble phosphate. Even Australia’s better soils are low in phosphate in comparison with most soils elsewhere in the world.

“Most phosphate has leached out, or been eroded by water and wind and deposited elsewhere, including in the Indian Ocean. Any phosphate left is sorbed onto soil particles and becomes tightly bound by iron, where even the fungal hyphae can’t get at it.

“Yet Banksias, Hakeas and Grevilleas growing in soils with almost no soluble phosphate have the same capacity to take up phosphate from soil as mycorrhizal species growing on normal soils. In addition, they manage to function at leaf phosphate concentrations around 10 times below that in most other plants. They are capable of developing concentrations of phosphate in their leaves that are orders of magnitude above the soil phosphate concentration in their root zone.

“Plants with proteoid or dauciform roots run on the smell of an oily rag, yet produce similar amounts of biomass to mycorrhiza-forming species. To get at insoluble phosphate, the plants have to mobilise it into solution.”

Lambers found that plant species with root clusters exude huge amounts of carboxylic acids into the surrounding soil: citrate, for most Proteaceae, and malonate, for some Cyperaceae. The acids liberate the phosphate and move it into solution. The plant’s root cells are studded with high-affinity phosphate transporters that capture phosphate ions and take the phosphate into the roots, an active process that consumes energy. Most of the phosphate is then transferred to the leaves and used for DNA, RNA and membranes and to allow photosynthesis and respiration.

The removal of phosphate by the roots creates a diffusion gradient that moves more phosphate into the root zone. Lambers says proteoid and dauciform roots are very short-lived, dying just two or three weeks after they form. Over time, dead proteoid roots form extensive, dense mats near the soil surface around the plant. Their expendability appears to reflect the substantial energy costs involved in growing new roots and synthesising large quantities of carboxylates. Between cycles in the Mediterranean southwest of WA, the plant stores the mined phosphate taken up in the wet winter in its stems, until it is required for its new leaves in spring and summer.

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Always on

Australia’s tropical and sub-tropical rainforests are home to ancient Proteaceae genera, most of which produce proteoid roots. Rainforest soils, just like WA’s heathland and woodland soils, are deeply leached and depleted of nutrients, so some of the rainforest ancestors of the heathland genera may have been pre-adapted to colonise phosphate-deficient soils.

In an unpublished study some years ago, one of Lambers’ colleagues in Queensland, Paul Reddell, grew Darlingia, Carnarvonia and Musgravea (an early relative of Banksia) at a range of phosphate concentrations. All produced proteoid roots, but a fourth, Placospermum, did not.

Placospermum is a rainforest relative of Persoonia, the only Proteaceae genera in WA that doesn’t produce proteoid roots. Instead, Placospermum forms mycorrhizas. Where the other three species continued to produce significant amounts of biomass at the lowest phosphate concentration, Placospermum grew extremely slowly. “We don’t understand how Persoonia obtains phosphate, because we can’t get them to germinate in sufficient numbers,” says Lambers.

Proteoid roots and organic acid secretion appear to have been early innovations in the family, that have been refined over tens of millions of years as the continent’s ancient landscapes were progressively depleted of phosphate. Lambers says most plants are potentially vulnerable to phosphate toxicity, but cease active uptake before their internal phosphate concentration reaches toxic concentrations. A homeostatic mechanism maintains a safe internal concentration very much below the 250-300 millimolar range that occurs in phosphate-sensitive hakeas.

But many plants that have evolved on extremely phosphate-deficient soils, including South African fynbos genera like Protea, Leucospermum and Leucadendron, have no ‘off’ switch. They continue to take up and concentrate phosphate in their leaves. Their growth slows and they turn sickly yellow; phosphate toxicity is irreversible and ultimately lethal.

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Peak phosphate

Western Australia’s unique flora is under siege from six different species of Phytophthora mould, including the notoriously destructive P. cinnamomi. Many Proteaceae genera like Banksia, Hakea and Grevillea are highly susceptible. However, this susceptibility is not linked to their cluster roots.

About 20 years ago, researchers discovered that spraying susceptible plants with phosphonic acid – phosphite – induces a protective response in vulnerable plants, that stops the motile Phytophthora in its tracks, without actually killing it. Low concentrations of phosphite induce protection, making aerial spraying of large areas of vegetation economically feasible.

But Lambers has serious reservations about the practice, pointing out that phosphite is readily converted to phosphate in soil. The Phytophthora risk is diminished, but at the risk of fertilising very nutrient-poor national parks or even causing large-scale phosphate toxicity. He points out the risk of disrupting whole ecosystems, making them prone to weed invasion and by killing off keystone plants. We urgently need an alternative for phosphate, he says.

Lambers suggests advanced breeding techniques could be employed to transfer genes from wild, root-cluster forming species to crop species in families like the Fabaceae, creating varieties that would be productive in phosphate-depleted soils.

“It’s not that plants with proteoid roots are doing something that other plants don’t do. They’re just genetically programmed to grow much larger numbers of shorter lateral roots simultaneously and to produce and release much greater quantities of organic acids.”

White lupins, widely grown by WA sandplain farmers, already produce cluster roots. So do a number of native pea genera, including some Kennedia, which Lambers and his colleagues are investigating as potential pasture species.

Alternatively, he says, homologues of the genes involved in such traits are likely to be present in crop species; in situ tuning might induce them to form root clusters.

Lambers sees an urgent need for science to develop crops for low-fertility soils. “We worry about the peak oil problem, but agriculture has a peak phosphate problem. By mid-century, we will exhaust half of all our readily accessible phosphate reserves, including rock phosphate. Crops can’t grow without phosphate, and there’s no substitute. We have to start recycling it, and making the most efficient use of it that we can.”