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B. I;. CARVER AND J. D. OWNBY
soil acidity. Reductions in forage and grain yields occur when soil pH ( 1 : 1 w/w
ratio of soil and water) falls below 5.0 to 5.2 (Westerman, 1987). To ensure a
margin of safety across soil types and cultivars, the minimum pH recommended
for wheat production is 5.5. In practice, however, producers often fall short of that
target pH, either in the subsurface or surface layers or both. This shortfall is experienced in wheat fields worldwide. Remediation of soil acidification can have
the appearance of prevention, correction, or tolerance. The latter constitutes the
theme of this chapter, not as an endorsement over other measures, but to recognize
a gradual crescendo over the last two decades in wheat literature emphasizing acid
The first objective of this chapter is to provide a fundamental appreciation for
the implications of soil acidity to wheat production on both sides of the equator,
including the nutritional disorders associated with phytotoxicity. This chapter's
intention is to bring to the view of plant scientists-including physiologists,
breeders, and geneticists-a problem founded on principles of soil science. Second, why some genotypes of wheat are more physiologically equipped than others
to tolerate soil acidity and how physiological adaptation is controlled genetically
will be explained. A central thesis to this discussion is that toxic factors in acid
soils initiate a cascade of stress responses in the wheat plant that demands multiplicity of tolerance mechanisms. Unfortunately, technology has not been applied
to the same level of sophistication for examining genetic mechanisms of tolerance
as for physiological mechanisms. When and how breeding solutions to acid-soil
stress can be achieved will also be discussed, with considerable detail given to the
arsenal of screening techniques available to the wheat breeder. The final objective
will be to promote the concept that sustainability in a soil-acidifying wheat production system is balanced by affordable management practices on one hand and
manipulation of genotype on the other.
OF SOIL ACIDITY
Soil acidity is determined by the amount of H' activity in soil solution and is
influenced by edaphic, climatic, and biological factors of natural occurrence
(Johnson, 1988). For example, soils which develop from granite parent materials
acidify at a faster rate than soils derived from calcareous parent materials. Sandy
soils with relatively few clay particles acidify more rapidly due to their smaller
reservoir of alkaline cations (buffering capacity) and higher leaching potential.
Excessive rainfall influences the rate of soil acidification depending on the rate of
percolation of water through the soil profile. Organic matter will decay to form
carbonic acid and other weak organic acids. The cumulative effect of these factors
is practically immeasurable over the course of a few years and, therefore, may
contribute relatively little to total soil acidity.
ACID SOIL TOLERANCE IN WHEAT
Vertical Distribution of pH in an Oklahoma Wheat Field
(3.0 Hectare) Continuously Cropped with Winter Wheat
and Sampled in a Grid Pattern to a 1.2-mDepth
" A 1 : I soil: water solution, as reported by Guertal(l993).
Soil acidity shows not only chronological variation but also spatial (horizontal
and vertical) variation. Highly weathered soils, such as Brazilian Oxisols, are
acidic throughout the profile. In contrast, Mollisols cropped with continuous winter wheat in Oklahoma develop phytotoxic levels of acidity confined to the surface
layer (Table I). The soil in this example is classified as a Pond Creek silt loam
(Fine-silty, mixed, mesic Pachic Argiustoll). It received annual applications of
anhydrous ammonia since 1982 and was limed 6 years prior to sampling. Typical
of acid soils of the Oklahoma wheat belt, surface (0-30 cm) pH values were
critically acidic, but subsurface ( 2 3 0 cm) mean pH values exceeded 6.5. Soil
acidity was also found in the top 30 cm for wheatland soils in southern New South
Wales (Fisher and Scott, 1987).
Soil acidity is often accelerated in the surface layer by certain cropping practices, e.g., repeated applications of nitrogen in excess of crop uptake. Net production of H occurs by natural processes, including nitrification of ammoniacal N:
+ 2H+ -+2NH,'
2NH4+ + 302 + 2NO2- + 4H' + 2H2O
+ O2 + 2N0,-
Some of this acidity is neutralized by NO,- uptake and the subsequent release
of OH -. Other compromising factors are the denitrification of NO3-, NH, volatilization, or NH,' uptake by the plant. Management practices which optimize
N-use efficiency and ultimately reduce the amount of NO,- lost by leaching could
slow the rate of acidification (Robson, 1989).
Soil acidification in the surface layer is also accelerated by the removal of basic
cations (Ca, Mg, K, and Na) in the harvested product. Different wheat cropping
B. F. CARVER AND J. D. OWNBY
practices increase or decrease the potential acidity caused by nitrification of applied N, depending on the relative amounts of forage, grain, and/or straw (and
therefore basic cations) removed. Removal of straw alone depletes basic cations
to the greatest extent and actually enhances acidification by nitrification (Westerman, 1987). Base depletion is less severe in forage removal (by grazing or hay)
and least severe in grain removal. Most multipurpose cropping systems (e.g.,
forage-plus-grain removal) reduce potential acidity caused by ammoniacal N application, albeit to different degrees depending on the excess basem ratio in different plant parts. Therefore, soil acidity will develop, and soil pH will decline, at
different rates depending on the cropping system. The severity of soil acidity increases as yields of vegetative or grain dry matter increase. This may explain why
soil acidity has reached unprecedented levels in some intensively managed soils
of Oklahoma and Kansas.
Acid soils are phytotoxic to wheat, not because of the deficiency or excess of
any one chemical element, but as the result of a complex of nutritional disorders:
deficiency of essential nutrients like Ca, Mg, and Mo; decreased availability of P;
and toxicity of Al, Mn, and H +.The relative importance of each of these factors
is difficult to generalize across soils with inherently different soil solution chemistry. The chemical and biological components of soil acidity, and their effects on
plant growth, are examined in a broader framework by Adams (1984) and Robson
(1989). That part of the literature which pertains exclusively to wheat deserves
some reiteration for the benefit of the reader with less familiarity. The more experienced reader might continue with Section I.C.
It is widely accepted that as pH decreases, both Al and Mn increase in solubility
and, consequently, in their relative toxicities (White, 1970; Marion er al., 1976).
The classic review by Foy et al. (1978) pushed Al toxicity to the center of attention among soil scientists, physiologists, and geneticists. However, the precise
form(s) of Al which restricts wheat root growth and subsequently hinders shoot
growth by interfering with nutrient uptake and transport remains a subject of debate. The various forms of potentially available Al, such as the relatively nonphytotoxic amorphous precipitates [AI,SiO,, AI(OH),, and AIPO,] and organically complexed forms of Al, or the potentially toxic inorganic monomers [Al t3,
AI(0H) + 2 , and AI(OH),+] have been summarized by Kinraide (199 1 ) and Blamey
and Asher ( 1993). Most Al in soils is present as solid, nontoxic forms. Typically
at pH > 5.5, exchangeable Al decreases dramatically with exception of exchange
sites associated with organic matter; consequently, Al toxicity also declines.
Baligar et al. (1992) found that the amount of Al extracted by 0.01 M CaCl, best
predicts wheat seedling root growth in a range of acid soils of the Appalachian
ACID SOIL TOLERANCE LN WHEAT
region. This result is expected if CaCl, primarily extracts only phytotoxic A1 species available in soil solution plus some exchangeable Al. Similar results can be
found in other acidic soils and plant species (de A. Machado and Gerzabek, 1993).
Immediate effects of A1 are observed in meristematic root tissue as elaborated
in Section 11, with root elongation ultimately retarded and root ion transport disrupted. The degree of retardation is subject to ameliorative effects of Mg, Ca, and
K (Kinraide and Parker, 1987; Tanaka er al., 1987; Baligar et al., 1992). Consequently, higher base saturation in surface horizons may lead to less inhibition of
root elongation compared to subsurface horizons. Aluminum-stressed wheat roots
typically appear shortened and thickened, while the effects of A1 toxicity on wheat
foliage are not as clearly defined and are often confused with poor N, P, Ca, or
Mg nutrition, and/or drought stress. Signs of A1 toxicity are unusually prostrate
growth, leaf chlorosis resembling N deficiency, and leaf or stem purpling similar
to P deficiency (Unruh and Whitney, 1986). Aluminum stress decreases total chlorophyll concentration and photosynthetic rate in wheat, but the decline in transpiration rate is the most severe (Ohki, 1986). The aluminum concentration in the
leaf may reach 0.3 mmol kg - when A1 is supplied in excessive amounts for
an extended period (0.30 mM for 28 days after transplanting seedlings; Ohki,
1986), but tissue concentrations in the foliage may not accurately reflect A1 stress
(Keisling et al., 1984). Because leaf concentrations constitute
absorbed Al, A1 tolerance per se in wheat is physiologically linked to root tissue
rather than to foliage (Zhang and Taylor, 1988).
The pruning effect of A1 stress on the root system elicits secondary responses
potentially detrimental to overall growth and development of the wheat plant. Absorption of relatively immobile elements like P is impaired in a root system reduced in surface area or weakened by A1 stress. Taylor and Foy (1985) demonstrated Al-induced nutrient reductions, and in some cases critical deficiencies, for
P, Ca, Mg, Fe, and Mn in wheat seedling foliage. Genetic differences in element
composition were not, however, convincingly linked to differences in A1 tolerance. Imbalance of Ca and Mg caused by A1 stress bears further implications to
nutritional quality of wheat forage for grazing ruminants. Thus, recent research
into mechanisms of Al phytotoxicity and tolerance has emphasized Al-induced Ca
and Mg disorders. For example, Huang et al. (1993) showed that A1 supplied in
solution culture reduced Ca uptake and translocation to different degrees in two
wheat genotypes differing widely in A1 tolerance. Long-term exposure to A1 was
previously shown to reduce Ca concentration in wheat forage (Huang and Grunes,
1992). The extent to which genetic variation in A1 tolerance is attributed to differences in Ca transport requires further study in a wider genotypic sample.
Aluminum stress may also intensify water-deficit stress under drought conditions, although direct evidence of this interaction is lacking in wheat. In another
cereal crop with generally less tolerance than wheat, water-deficit stress magnified
the effect of Al stress on two barley cultivars differing in A1 tolerance (Krizek and
B. F. CARVER AND J. D. OWNBY
Foy, 1988). Vegetative growth of the Al-tolerant cultivar was much less reduced
than that of the sensitive cultivar. Likewise in soybean, Glycine max (L.) Merr.,
the combined effect of water-deficit stress and A1 stress on leaf water status exceeded predictions based on additive effects (Goldman er al., 1989a). Intuitively,
root systems impaired by A1 stress have limited ability to withstand drought stress.
Goldman er al. (1989b) recommended that soybean breeders select for A1 tolerance when developing drought tolerant cultivars because A1 tolerance may impart
some degree of drought tolerance in areas limited by low rainfall and subsoil
acidity. Testing of similar hypotheses are apparently lacking in wheat.
Aluminum activity in soil solution may not totally explain phytotoxicity of soil
acidity. The availability of Mn may exceed basal plant requirements for enzyme
activation in the tricarboxylic acid cycle and for other physiological functions.
Toxicity typically develops in acid soils with pH 6 . 5 or at higher pH values
when soils are poorly drained or waterlogged, conditions which promote reduction of Mn4+and Mn3+to the more available Mn2+(Westerman, 1987). Thus, it
is possible to find symptoms of Mn toxicity at a pH too high to cause A1 toxicity
(Foy, 1983). Unlike Al, which is an integral part of the clay structure in acid soils,
Mn is not part of the clay structure and originates in Mn-oxide parent materials or
as an impurity. Thus, in addition to pH, total Mn content inherent to the soil
largely determines potential Mn toxicity.
Visual symptoms of Mn toxicity recorded for wheat under greenhouse conditions include stiffness and stunting of leaf tissue, with general chlorosis and some
leaf necrosis, purpling, white flecking, and tip burn (Keisling et al., 1984; Ohki,
1984). In contrast to A1 stress, Mn toxicity is primarily expressed in the foliage
and may not appear immediately following exposure to toxic amounts of Mn.
The Mn concentration for wheat shoot tissue associated with a 10% reduction in
growth or activity (critical toxicity level) is approximately 7 to 8 mmol kg - I
(Fales and Ohki, 1982; Ohki, 1985; Keisling er al., 1984); this level increases
almost threefold for leaf photosynthesis, chlorophyll concentration, and transpiration (Ohki, 1985). Why Mn-induced stress reduces dry weight production before reducing photosynthesis and transpiration is not documented, but may be
explained by a concomitant increase in the maintenance component of respiration
in response to Mn toxicity. Tissue Mn concentrations which exceed the critical
toxicity level also cause reductions in Ca and Mg concentrations, with potential
consequences to forage digestibility (Fales and Ohki, 1982). In turn, Mg availability influences the severity of Mn toxicity.
c. SEVERITY AND EXTENTOF SOIL ACIDITY
Once considered a problem confined to tropical agricultural regions or high
rainfall areas with highly weathered soils, soil acidity now attracts global attention
ACID SOIL TOLERANCE IN WHEAT
in nearly every major wheat production region. Wheat producers must contend
with acid soils in the United States, Australia, Canada, the Southern Cone region
of South America, the Carpathian basin region of Europe, Central Africa, and,
more recently, South Africa.
The traditional view in the United States is that soil acidity is the most detrimental to crop production in the southeastern states. For wheat production in particular, it is the more densely cultivated region of the southern Great Plains where
soil acidity takes its toll on vast acreages. Although virgin soils were slightly
acidic (pH 5.5-6.5), surface soil pH has gradually declined to 4.0 or below over
the last 40 years under continuous wheat production. The severity of acidity is
greater in wheatland soils of the Southeast, but the number of cultivated wheat
hectares impacted by acid soils is greater in the southern Great Plains. A statewide
soil test survey revealed critically acid conditions (pH <5.0) in the surface layer
of 15% of the total wheat area of Oklahoma (Johnson, 1986). This would equate
to about 0.5 million hectares of hard red winter wheat in Oklahoma alone (authors’ estimate) which suffer potential production losses due to soil acidity. Soil
acidity in the southern Great Plains extends across Oklahoma, from northcentral
Texas to southcentral Kansas, and reduces production primarily due to toxic
amounts of Al and, to a lesser extent, Mn. Soil test surveys conducted in Kansas
indicated four intensively cropped counties in southcentral Kansas with alarming frequencies of low pH soils (Unruh and Whitney, 1986). The actual pH level
is highly variable in this tri-state region, largely depending on liming practices
adopted by different producers or landowners.
Like the southern Great Plains, mildly acidic soils of the eastern edge of the
wheat belt in southern Australia have become increasingly acidic over the past
40 years (Fisher and Scott, 1987; Chartres et al., 1990; Scott et al., 1992). Some
1 million hectares devoted to wheat production in the Albury, Wagga, and Cootamundra districts of New South Wales are threatened by acid soils and A1 toxicity.
More than one-third of the total agricultural land area in New South Wales has
severely acidic surface soil with pH <4.5 (Scott et al., 1992). Also affected
by acid conditions are the eastern wheat areas of Western Australia (Davidson,
1987). Acidity is not necessarily confined to the surface layer, depending on soil
Cultivated soils have developed surface acidity throughout Alberta and northeastern British Columbia (Penney et al., 1977) in northwest Canada. Extensive
subsoil acidity also occurs in the Peace River region of Alberta and British Columbia (Zale and Briggs, 1988). To what extent soil acidity in this region influences
wheat production specifically could not be determined from these reports, but a
review by Briggs and Taylor (1994) indicates that 5.0 million hectares of Canadian arable soil are acidic, with over 2 million in western Canada where wheat is
In Europe, A1 tolerance is desired in the intensively cropped wheat areas of
B. F. CARVER AND J. D. OWNBY
Hungary (Bona and Carver, 1992) and in Poland, where 60% of all agricultural
land is critically acidic (Aniol, 1984b). Rengel and Jurkic (1993) recognized the
importance of A1 toxicity to wheat production in Croatia and Yugoslavia, where
about 50% of all agricultural land is affected.
Another major wheat production region limited by increasing soil acidification
is composed of the three principal wheat producing areas of South Africa. Based
on a personal communication (1994) with 0. J. Bosch, Grain Crops Institute,
Bethlehem, approximately 0.4 million hectares of wheat produced in the summer
rainfall region of South Africa are considered critically acidic with pH(KC1) <4.5.
Most of those hectares are in the higher rainfall areas. In the winter rainfall region
of South Africa, another 0.07 million wheat hectares have critical soil acidity.
Aluminum toxicity is the primary limiting factor to wheat production in acidic
soils of South Africa; Mn is not normally available in toxic quantities. The severity and extent of soil acidity in worldwide wheat production warrants continued
investigation of the plant’s defense mechanisms against low-pH-induced stresses
and the genes which regulate those mechanisms.
11. PHYSIOLOGY OF ALUMINUM AND MANGANESE
TOLERANCE IN WHEAT
As discussed earlier, reduction in wheat growth and yield in acidic soils is generally a consequence of A1 and/or Mn toxicity. The chemistry of these two metals
is quite different, as is their role in plant development. Manganese is an essential
element whereas Al is not. Mechanisms by which plants tolerate toxic levels of A1
and Mn are likewise different. Wheat cultivars tolerant of one metal are not necessarily tolerant of the other. The next section describes physiological mechanisms by which plants may tolerate A1 and Mn, with particular emphasis on insight gained from recent work with wheat.
The primary response to Al stress in wheat occurs in roots, where reduced elongation at the tip, followed by swelling and distortion of differentiated cells, as well
as root discoloration, has been described for a wide variety of taxa (Foy et al.,
1978; Bergmann, 1992, pp. 282-289). Within meristematic and root cap cells, A1
toxicity is associated with increased vacuolation and turnover of starch grains (de
Lima and Copeland, 1994), as well as disruption of dictyosomes and their secretory function (Bennet et al., 1985; Puthota et al., 1991). In Zea mays L., Bennet
et al. (1985) observed that cortical cells of Al-damaged roots were swollen, with
ACID SOIL TOLERANCE IN WHEAT
grossly distorted walls; rupture of the cells of the epidermis and outer cortex was
noted at high Al concentrations. The ability of Al-damaged roots to synthesize
and translocate growth-promoting hormones such as cytokinins does not appear
to have been investigated.
An understanding of the dynamics of root growth inhibition by Al is important
in designing experiments to elucidate Al tolerance mechanisms. Recent studies
have shown that reduction in elongation of Al-challenged wheat roots commences
after a lag period that may be as short as 2 hr (Ownby and Popham, 1989; Ryan
ef al., 1992). Parker (1 994) has concluded from analysis of wheat root growth that
there are two responses to Al: an initial “acute” inhibition of growth that is followed by a later “chronic” A1 effect on root growth. In his study, some, but not
all, wheat cultivars became acclimated to low levels of Al and resumed growth
after the initial shock. Surprisingly, the acclimation phenomenon appeared in Alsensitive cultivar ‘Scout 66’ as well as in Al-tolerant ‘Atlas 66,’ and no correlation
between acclimation and Al tolerance was observed. The concept of acute vs
chronic growth inhibition by Al is useful in evaluating various approaches to the
study of Al toxicity. As Parker ( 1994) noted, short-term experiments by physiologists may reveal mainly acute effects of Al on growth, while long-term field work
and breeding studies are more likely to observe chronic phytotoxicity of Al, which
could have a different physiological basis. Likewise, short-term tests for Al tolerance such as root growth (Kerridge et al., 1971) and hematoxylin staining (Polle
et af.,1978) may not invariably predict long-term performance of crops in acid
soils. Indeed, examples of this have been observed (Scott and Fisher, 1989).
This concept may also be useful in resolving what appears to be contradictions
in the plant response to Al. Among the effects of Al that often appear after its
initial effect on growth are inhibition of DNA synthesis (Wallace and Anderson,
1984), alteration of cell membrane potential (Kinraide, I988), and reduction of
root apex H + efflux (Ryan ef al., 1992). These effects eventually contribute to
cessation of root growth (i.e., the chronic effect) but they appear to succeed an
initial response with which they may not be primarily involved.
Two major unresolved questions about Al in plants concern its chemical form
and cellular distribution. The general assumption that Al 3 + , the major form of
Al,,,,,,,,at pH <4.75, is phytotoxic has been confirmed in wheat (Parker et al.,
1988). However, as Taylor (1991) pointed out, the level of A13+that may exist in
cell cytoplasm can be no greater than 10 l o M , and is probably much lower due
to inorganic phosphate and other ligands. The results of studies in virro that assume reaction with Al 3 + thus may not apply to cytoplasmic conditions. Mononuclear hydroxy-Al does not appear to be very toxic in wheat but was suggested to
be more toxic than A13+ in dicots (Kinraide and Parker, 1989; but see Kinraide,
199 I). The polynuclear hydroxy-Al (A1 species may be a major toxic Al species
in the root apoplast. Parker et al. (1989) reported that Al,, was as toxic to AItolerant wheat cultivar ‘Seneca’ as to Al-sensitive cultivar ‘Tyler’; however, Kin~