boron toxicity tolerance in crops

854 WWW.CROPS.ORG CROP SCIENCE, VOL. 48, MAY–JUNE 2008

REVIEW & INTERPRETATION

On a cold but sunny day in February 1985, when I (S.K. Yau) was taking notes on barley (Hordeum vulgare L.) lines

developed by us (the Barley Breeding Program of the International Center for Agricultural Research in the Dry Areas [ICARDA]) at Bouieder (rainfall around 230 mm) in Syria, I saw strange symp-toms on many of the newly developed lines, but not on the local Syrian landrace check. I wrote on my notebook wondering what type of disease could develop on barley so early in the season on such a bitterly cold, treeless steppe.

In spring 1992, Tony Rathjen from South Australia, on a visit to ICARDA, reported that he had observed boron toxicity (BT) symptoms on barley growing at the Breda substation (270 mm rainfall). The tiny brown spots on the leaf samples that he took for us did not convince me at the time that the problem was not of pathogenic origin. It was not until the fall of 1992, after I tested several barley lines in pots to which diff erent amounts of boric acid were added, that I was fi nally convinced that the symptoms we had observed were indeed BT.

Boron Toxicity Tolerance in Crops: A Viable Alternative to Soil Amelioration

Sui Kwong Yau* and John Ryan

ABSTRACT

Research on the problems of excessive soil B has

increased considerably in the past two decades,

especially in the dry areas of the world such as

the Mediterranean region and parts of Austra-

lia. The objectives of this review are to promote

awareness of the widespread occurrence and

importance of B toxicity (BT) in dry areas, and to

review the availability of BT-tolerant germplasm

and progress in breeding cultivars with BT toler-

ance. The importance of BT was not adequately

recognized until the 1980s, when scientists dis-

covered that BT caused signifi cant crop yield

reductions in South Australia. We offer sev-

eral reasons for this belated awareness before

describing the areas reported to have high-B

soils in the world and reviewing the occurrence

of two contrasting types of BT symptoms. In the

fi eld, BT in crops usually is more prominent after

drought, indicating that both BT and drought

tolerance are needed in crops for dry areas hav-

ing high levels of subsoil B. The interaction of

BT with salinity and the levels of other nutrients

such as Zn and N are also discussed. As it is

neither practical nor easy to detoxify high-B soil

by agronomic means in most circumstances,

selecting or breeding crop cultivars with high

BT tolerance is the only practical approach to

increase yields on high-B soils. Extensive sur-

veys of germplasm in different crops have been

performed, and a list of some BT-tolerant lines

or cultivars is presented. Finally, we review the

progress in breeding for BT tolerance, which has

been achieved with varying success in several

common crops. We believe that the shift from

soil intervention to plant adaptation to solve an

intractable crop nutrition constraint represents

a new paradigm in the agronomic sciences.

S.K. Yau, Faculty of Agricultural and Food Sciences, American Univ.

of Beirut, P.O. Box 11-0236, Beirut, Lebanon; J. Ryan, International

Center for Agricultural Research in the Dry Areas (ICARDA), P.O.

Box 5466, Aleppo, Syria. Received 1 Oct. 2007. *Corresponding

author ([email protected]).

Abbreviations: BT, boron toxicity; ICARDA, International Center

for Agricultural Research in the Dry Areas; WANA, West Asia and

North Africa.

Published in Crop Sci. 48:854–865 (2008).doi: 10.2135/cropsci2007.10.0539© Crop Science Society of America677 S. Segoe Rd., Madison, WI 53711 USA

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CROP SCIENCE, VOL. 48, MAY–JUNE 2008 WWW.CROPS.ORG 855

INTRODUCTIONResearch in soil fertility, plant nutrition, and plant breed-ing has identifi ed and largely eliminated nutrient con-straints, especially in the developed world. Besides, the supply and effi cient use of fertilizers have been enhanced, and the yield potential of varieties to better nutrition has been raised. The predominant emphasis of soil and agro-nomic research has been on rectifying nutrient defi ciencies in an economically and environmentally benign manner. Eff orts to deal with soil conditions where nutrients occur in nature in excessive amounts such as to impede crop growth were considerably less than those dealing with defi ciency. This dichotomy is well illustrated in the case of B, whose defi ciency and the implications for crop pro-duction have been the focus on much research globally for many decades. In sharp contrast, only a few standard textbooks (e.g., Bradford, 1966; Marschner, 1986) made reference to the phenomenon of BT, refl ecting the paucity of research publications on the subject and a general lack of awareness of the problem.

Boron is one of the eight essential micronutrients for healthy crop growth and its defi ciency is a widespread problem in relatively humid areas of the world (Gupta, 1979). Some early surveys (Berger, 1962) have shown that defi ciency was common throughout the United States. The preponderance of research papers in the past 50 yr have dealt with various aspects of B related to defi ciency; for example, geographic distribution, chemical reactions and equilibriums, functions in plants, mechanisms of plant uptake, soil and tissue testing, and fertilization (Mortvedt et al., 1991). Increasingly, the growing body of research and educational literature on soils and crop nutrition refl ected the accumulating knowledge on B defi ciency and its wider implications.

Relative to B defi ciency, the importance of an excess of soluble B in the soil that gave rise to the phenomenon of BT in limiting crop growth and yield was realized only recently (1980s), despite the fact that it was reported to occur in the western United States many years ago from irrigation waters containing excess soluble B (Oertli, 1960; Ryan et al., 1977). Boron is unique as a micronutrient in that the threshold between defi ciency and toxicity is nar-row (Mortvedt et al., 1991). Despite the fact that one of the fi rst surveys of soils on a global scale indicated that BT might be a problem, especially in dry regions of the world (Sillanpaa, 1982), the phenomenon remained largely unap-preciated by soil and crop scientists—and ignored in the literature. For instance, only a fl eeting reference, with-out any elaboration, is made to BT in the celebrated soils textbook of Brady and Weil (1999), while no mention is made of BT in any issue of Crop Science since its inception, despite the fact that many papers have dealt with genetic variation in crop nutrition. Indeed, of the more than 600 papers presented at the 15th International Plant Nutrition

Colloquium in China (Li, 2005), only one paper dealt with BT, and that was in relation to microorganisms.

However, a relatively recent publication by Cartwright et al. (1986) was a milestone in catalyzing the awareness of BT in that it showed a signifi cant yield reduction in com-mon wheat (Triticum aestivum L.) attributed to excess B; others (Yau and Saxena, 1997; Yau et al., 1996) confi rmed these observations. Before Cartwright’s paper (1986), there were seven papers on BT in crops between 1976 and 1985, followed by nine papers in the decade immediately after that. Not surprisingly, following the increased research activity on BT, this number increased exponentially in the past decade to 103.

Given the dearth of information on BT in the general literature, and the growing recognition of the BT prob-lem in international agriculture, we have attempted in this paper to give momentum to promoting this awareness. Our review on BT is not intended to be a comprehensive one, but rather is a selective one. Readers who are inter-ested in diagnosis of BT in plants and soils, amelioration of B-laden soils, and physiology and genetics of tolerance to BT are referred to the review by Nable et al. (1997). Ear-lier reviews by Gupta et al. (1985) and Gupta (1993a) have concentrated on soil and environmental factors related to B. This article refl ects our combined experience in both Australia and the Mediterranean region, where the prob-lem of BT is endemic. The review by a plant breeder and a soil scientist refl ects a paradigm shift from soil ameliora-tion to breeding for crop tolerance.

BRIEF HISTORICAL ACCOUNT ON BORON TOXICITYBoron toxicity in fi eld crops was probably fi rst reported in 1933 on barley in the United States by Christensen (1934). However, it was not until the discovery in 1983 and the following years of how widespread the BT problem was in South Australia (Cartwright et al., 1984; Wayne, 1986) that serious concern arose, resulting in eff orts to tackle the problem in Australia and in other dry areas of the world. In West Asia–North Africa (WANA), research on BT started in 1992.

Many reasons contributed to the obscurity of BT in the past:

1. High soil-B concentrations commonly occur in the subsoil, which generally coincides with the depth of moisture penetration in the profi le, or the wetting front (Cartwright et al., 1984, 1986; Ryan et al., 1998). As routine soil sampling only involves the top 0- to 20-cm layer of the soil, the problem of high-B soils escaped attention of scientists for a long time. Patterns of water-soluble B distribution with profi le depth are illustrated (Fig. 1) for ICARDA’s driest site for barley testing (Boueider) in Syria. Eight out of the 10 profi les show that B concentrations increase substantially from


comparing WANA with Western Europe, where B defi ciency is common.

5. The fact that phloem mobility of B varies dramati-cally with species (e.g., cereals vs. some fruit trees) and causes profoundly diff erent BT symptoms could have confused earlier workers. This point will be further discussed later.

AREAS WITH NATURALLY OCCURRING HIGH-BORON SOILS

Based on Soil Analysis

Boron toxicity occurs mainly in dry areas, especially in alkaline soils (Bradford, 1966; Marschner, 1986; Leyshon and Jame, 1993). This is in contrast to B defi ciency, which is more of a problem in high rainfall areas, because soils formed in humid climates are more prone to depletion of relatively mobile elements such as B (Harmsen and Vlek, 1985). A recent study (Ryan et al., 1998) that examined B distribution profi les across a mean annual rainfall gradi-ent (196–471 mm yr–1) in the cereal-production zone in northwestern Syria clearly illustrated this pattern of B dis-tribution. The wetter sites had low levels of B through the profi le, while the drier sites tended to accumulate poten-tially toxic levels, which increased with profi le depth. It is apparent that in dry areas the limited precipitation does not leach the B down below the root zone, and, as alkaline soils adsorb more B than acid soils (maximum adsorption of B around pH 9), only a small fraction of the free B is leached out of the profi le or root zone.

There are a few causes leading to high B levels in soil solution (Bradford, 1966; Leyshon and Jame, 1993). The two common causes in WANA are (i) soils inherently high in B, such as those formed from sea sediments or volcanic origin, and (ii) use of irrigation water from deep wells high in B (Chauhan and Asthana, 1981; Keren and Bingham, 1985). Causes of BT in other areas may include accidental applications of excess B in treating B defi ciency (Gupta and Gupta, 1998), application or disposal of fossil combustion residues such as coal fl y ash, and application or disposal of B-containing waste materials such as sewage sludge. Based on the climate of the area and origin of the soils, the occurrence of high-B soils may be predicted to a certain extent; for example, areas in southern Australia (marine origin, alkaline soils) and Sicily and the northern Andean region (volcanic origin) (Moody et al., 1988).

Boron toxicity evidently occurs in diff erent geo-graphic areas of the world. In the United States, it occurs widely in California, especially in the southern part of the state (Kelley and Brown, 1929), the Sacramento Valley (Branson, 1976), and the San Joaquin Valley (Ashworth et al., 1985). Not surprisingly, many papers on BT, ranging from the earliest (Eaton, 1935; Oertli, 1960) to the signifi -cant fi ndings on B mobility (Brown and Hu, 1996), came

around 2 mg kg–1 to around 8 mg kg–1 or higher at or below 30-cm depth (Ryan et al., 1998).

2. Boron toxicity symptoms in wheat are not conspicu-ous and could be confounded with symptoms caused by other abiotic stresses like drought or salinity. When symptoms are easily seen, as in barley, they were initially thought to be symptoms caused by fungal diseases (Christensen, 1934).

3. In WANA, landraces grown in high-B areas usually are BT tolerant with little symptom expression.

4. There is less research in dry areas relative to well-watered, fertile regions. This is especially true when

Figure 1. Patterns of depthwise distribution of water soluble B

from 10 profi les at Boueider, a dry site in northern Syria (Ryan et

al., 1998).


from California. High-B soils are also found in the Lower Rio Grande Valley of Texas, where there are high indig-enous B levels and where well water also contains high B levels (Cooper et al., 1955).

Probably the country of greatest signifi cance as far as BT is concerned is Australia. After high subsoil B concentrations were found in South Australia (Cartwright et al., 1984), soil surveys of B levels with depthwise sampling were carried in the whole province. From the maps produced, it can be seen that most of the northern, drier regions have B concentra-tions (CaCl

2 soluble) >15 mg kg–1 at 50- to 100-cm depths

or shallower. A similar situation was found in nearby areas of Victoria (i.e., southern Mallee, northern Wimmera, and central Wimmera) (Hobson et al., 2006). In Western Austra-lia, about 40% of the surveyed crops in the <350 to 450 mm annual average rainfall zones developed BT symptoms, and concentrations of mannitol-extractable B (soluble fraction) in subsoil varied widely between 0.7 and 130 mg B kg–1 soil (Brennan and Adcock, 2004).

In contrast to Australia, the WANA region is more ecologically diverse, having areas adequate in B (Khan et al., 1979), defi cient in B (Rashid et al., 1994), as well as high in B. For example, soil samples collected in Iraq, Syria, and Turkey (Central Anatolian Plateau) had high B levels (Sillanpaa, 1982). A soil survey in northeastern Iraq found an average hot-water soluble B of 2.4 mg kg–1 (from traces up to 13.3 mg kg–1), with the levels increas-ing from north to south, reaching a maximum average in Sulaimaniyah of 5.6 mg kg–1 (Amadi and Lazim, 1989). There are relatively high B levels in the Iraqi soils as they were derived from recent marine deposits, and the high pH and high CaCO

3 and clay content, together with the

dry weather, enhance B fi xation (Al-Khafaji, 1995).As pointed out earlier, high subsoil B concentrations

occur at dry sites in Syria (Ryan et al., 1998). Sites with high-B soils were identifi ed recently in Turkey (Torun et al., 2003). Based on a survey on BT symptoms in bar-ley crops, Avci and Akar (2005) claimed that BT is not a widespread problem in the Central Anatolia and Transi-tional Zones of Turkey, as symptoms were not observed in 79% of the samples. Fortunately, they (Avci and Akar, 2005) realized that they had underestimated the problem since farmers were growing BT-tolerant barley cultivars.

In Israel, muck soil contains exceptionally high water-extractable B (5–24 mg kg–1) and the Terra Rossa (Rhodox-eralf ) soils contains above-average level of water-soluble B (>3.0 mg kg–1) (Ravikovitch et al., 1961). Besides the south-western United States, southern Australia, and the Middle East, high-B soils also occur in Sicily (Moody et al., 1988). According to literature cited by Nable et al. (1997), high soil B is to be found in diverse agro-ecologies such as the west coast of Malaysia, valleys along the southern coast of Peru, the Andes foothills in northern Chile, in solonchaks and solonetz soils of the former USSR, and ferrasols in India.

Based on Irrigation Water

Underground water for irrigation contains toxic amounts of B in arid or semiarid states of India, such as Uttar Pradesh, Rajasthan, Haryana, Punjab, and Gujrat (Chau-han and Asthana, 1981). Underground water for irriga-tion in the western desert of Egypt was shown to be high in B (Elseewi, 1974). Boron toxicity has been reported on irrigated peas (Pisum sativum L.) in Spain (Salinas et al., 1981) and Arizona (Ryan et al., 1977), on kiwifruit (Actinidia deliciosa L.) irrigated with high-B water in north-ern Greece (Sotiropoulos, 1997), and on rice (Oryza sativa L.) using irrigation water from deep wells containing a high-B concentrations at Los Baños and Albay in the Phil-ippines (Dobermann and Fairhurst, 2000). Besides wells, water from creeks fl owing through outcrops of borate deposits was found to contain high levels of B in southern California (Kelley and Brown, 1929).

Based on Toxicity SymptomsBoron toxicity symptoms were identifi ed, usually in barley, in many countries of WANA; for example, areas around Aleppo in Syria (Yau et al., 1994b), Anatolian Plateau of Turkey, and on the northwest coast of Egypt. In Tur-key, BT symptoms were detected in farmers’ fi elds in the Ankara, Konya, and Esksehir areas, and at the Hamidiye Research Station near Eskisehir (A.J. Rathjen, personal communication, 1992; Yau et al., 1996). Toxicity was also reported at the research stations of Tiaret, Saida, and Sidi Bel Abbes in Algeria (Yau et al., 1997a), northwest coast of Egypt (A.J. Rathjen, personal communication, 1992), Sinai of Egypt, Libya, Morocco, and Tunisia (Yau, 1997).

Screening based on BT symptom severity also sug-gested that BT could be widespread in West Asia, as some of the dominant varieties are tolerant to BT (refer to Table 1; Yau et al., 1994a). A glasshouse screening of 226 bar-ley lines from the Central Anatolian Plateau of Turkey revealed that most lines were fairly tolerant to BT (Yau et al., 1996). Other studies showed that one-fi fth of the 50 Iraqi accessions were BT tolerant, and the tolerant accession ‘ICB 104041’ from Afghanistan had signifi cantly higher straw yield under conditions where BT occurred (Yau et al., 1995a). Barley accessions from Iran and Afghanistan were the most BT tolerant among seven WANA countries (Yau, 2002a). Other studies on bread wheat (Moody et al., 1988), peas (Bagheri et al., 1994), durum wheat (T. durum Desf.) (Yau et al., 1998), and lentil (Lens culinaris Medik.) (Yau and Erskine, 2000) have also shown germplasm from Afghanistan to be BT tolerant, indicating that high-B soils occur widely in that country.

The outcome of screening for BT tolerance in barley varieties and accessions from WANA and Europe supports the hypothesis that high-B soils are common in WANA and that B defi ciency is common in European soils. In one study, most varieties from West Asia showed little BT symptoms,


but all the European varieties in the test had severe symptoms (Yau et al., 1995a) and had a higher reduction in shoot growth (Yau, 2002a). Screening 420 random barley accessions from seven European countries and seven WANA countries fur-ther showed European accessions to be less tolerant to BT than WANA accessions (Yau, 2002a). Diff erential responses of barley lines to high-B soils were shown to cause genotype by environment interaction in grain yields across diverse environments in WANA and Europe (Yau and Tahir, 1996). The lower BT tolerance of European germplasm could be one of the reasons why such lines or cultivars are not adapted to WANA, thus providing an example of edaphic adaptation on a macro scale.

PHLOEM MOBILITY OF BORONThe classical BT symptoms are necrosis or chlorosis of leaf tips and margins found in older leaves (Fig. 2) (Gupta, 1993b). These symptoms arise as B is immobile in these species, causing B accumulation in the older leaves. There are progressively lower B concentrations in younger leaves and fruits. From what we have seen and read, all common WANA fi eld crops such as barley, bread wheat, durum wheat, lentil, chickpea (Cicer arietinum L.), faba bean (Vicia faba L.), vetch (Vicia spp.), and alfalfa (Medicago sativa L.) have this type of BT symptoms.

However, the symptoms of BT reported by Bradford (1966) for stone-fruit trees were diff erent from the classical symptoms. Instead, there was twig dieback, gum exuda-tion in leaf axils and buds, and appearance of brown, corky lesions along stem and petioles (Brown and Hu, 1998b), or cracking and splitting of the bark in species of Prunus

(Woodbridge, 1955). Others also had reported similar BT symptoms in species of Malus and Pyrus (Hansen, 1948; Choe et al., 1986). As expected, many horticulturalists would not recognize that these symptoms were due to BT; these symptoms could have been easily mistaken for other diseases and physiological disorders.

This diff erent type of BT symptoms expressed by many fruit trees is caused by high B mobility in the phloem (Brown and Hu, 1996). This mobility occurs as a result of utilizing polypols (complex sugars), such as sorbitol, that has a high affi nity to bind B as a primary photosynthetic metabolite. These metabolites are formed in the photosynthetic tissues and are transported to currently active sinks such as growing shoots and fruits. As a result of this mobility, B accumulates in the tissue and BT symptoms consequently appear in the mer-istemic regions or fruits, but not in the mature leaves (Brown and Hu, 1998b). According to Brown and Hu (1998a), fruit trees such as apple [Malus domestica (Borkh.) Borkh.], almond (Prunus dulcis (Mill.) D.A. Webbe], apricot (Prunus armeniaca L.), cherry [Prunus avium (L.) L.], grape (Vitis vinifera L. and others), loquat [Eriobotrya japonica (Thunb.) Lindl.], olive (Olea europaea L.), peach [Prunus persica (L.) Batsch], pear (Pyrus spp.), plum and prune (Prunus spp.), and pomegranate (Punica grana-tum L.) express BT symptoms as twig dieback. Besides fruit trees in the Prunus, Malus, and Pyrus genera, vegetable such as celery (Apium graveolens L.) and many ornamental species, for example, bearberry (Cotoneaster dammeri C.K. Schneid.), lady’s glove (Digitalis purpurea L.), and Cape jasmine (Gardenia jasminoides Ellis), were found to have B phloem mobility as well (Brown et al., 1999).

Such drastic diff erences in B phloem mobility and expression of BT symptoms has signifi cance for the diag-nosis of BT. Old leaves are suitable for determining BT only in B-immobile species, but not for species in which B is mobile. For the latter, young apical leaves or fruit tis-sues is needed. In California, for almonds, there is a wide-spread use of B in the hull as a determinant of B status in that stone fruit (Brown and Hu, 1998b).

INTERACTION OF BORON TOXICITY WITH OTHER FACTORS

Drought

That high B levels usually occur in subsoil explains why the problem of BT was usually discovered after a drought (Cart-wright et al., 1986). According to Adcock et al. (2007), sub-soil limitations, like BT, may be responsible for poor crop yield on the alkaline to neutral soils in southeastern Australia by reducing root growth, especially in drier seasons. This was clearly illustrated by Holloway and Alston (1992), in whose study subsoil was treated with a range of B and salt. The added B had a greater eff ect than salt in reducing wheat root density with depth; at a high B level, few roots pen-etrated below 0.4 m. Associated with this decrease in root

Table 1. Boron-toxicity symptom scores and dry weight

change in B25† for two contrasting groups of winter or fac-

ultative barley in the Barley High Elevation Adaptation Yield

Trial (Yau, 2002a).

Entry name OriginB-toxicity

symptom score‡

Dry wt. change§

%

Tolerant group

Baluchistan Pakistan 1.8 +26

ICB 104041 Afghanistan 2.3 –16

Alger/Ceres North Africa 0.8 +19

Tokak Turkey 0.8 –23

Zarjou Iran 2.0 +27

Sensitive group

Cyclone Russia (Saratov) 3.3 –47

Lignee 527 France 6.5 –31

Plaisant France 2.8 –74

Robur France 5.5 –14

Victoria Romania 3.0 –64

†Soil to which 25 mg B kg−1 soil has been added.

‡0–10 scale: 0 = no symptom, 10 = covered with symptoms. Symptoms consisted

of dark brown spots or blotches besides chlorosis, fi rst appeared at or around the

leaf tip in older leaves then developed along the leaf edges down to the leaf base.

§From normal soil to B25 soil.


density with depth, soil water increased in the lower part of the profi le. This led Holloway and Alston (1992) to con-clude that in seasons when the upper soil is frequently wetted, restriction for roots to penetrate deeper soils may not reduce yield. However, in seasons with low rainfall, the deleteri-ous eff ects of B and salt on root growth may prevent subsoil moisture from being used.

Since drought has such a big eff ect on BT, our group expanded the research. In the preliminary study, there was no interaction between the eff ects of terminal drought and BT on barley grain yield and many other agronomic characters (Yau, 2001). As drought may occur at diff erent growth stages, and there are diff erences among varieties in BT tolerance, the next study involved early, midsea-son, and terminal droughts and compared two contrasting genotypes: one BT tolerant and one drought tolerant but susceptible to BT (Yau, 2002b). In this follow-up experi-ment, signifi cant B by drought interaction was detected with root growth in the subsoil, straw B concentration, and straw and biological yields for the BT-susceptible gen-otype, but not for the BT-tolerant line. Clearly, both BT tolerance and drought tolerance are needed in dry areas having high levels of subsoil B.

One may wonder why in most of the pot experiments on BT, excess B was introduced right from germination, although B in arid areas tends to accumulate in the subsoil, coinciding with the depth of moisture penetration. Depend-ing on environmental conditions, plant roots may not reach this layer, or if they do, it takes time after germination. In a study on this issue by Riley and Robson (1994), although B was added at three diff erent growth stages, B was top-dressed; creating an artifi cial situation that was diff erent from the fi eld conditions. To mimic the fi eld situation bet-ter, tubes were split into half horizontally to study the eff ects of three patterns (normal soil in top and bottom sections; normal soil in top but high B soil in bottom section; high B soil in both sections) and three times of B application (join-ing the bottom section to the top section) on the develop-ment, growth, and yield of two barley lines in a follow-up study (Yau, 2004). Subjecting the pot plants to high-B soils from germination to maturity exaggerates the eff ects of B on crops in the fi elds, but high subsoil B levels can cause yield reduction even when roots reach it as late as the boot stage. This fi nding was supported by fi eld results of Brennan and Adcock (2004) which showed that although BT symptoms developed only at or after the boot growth stage in ‘Stirling’ barley grown on a duplex soils (those with a light-textured topsoil overlying a clay subsoil) with high concentrations of mannitol-extractable B in the subsoils (>30 cm), there were small reductions (up to 10%) in grain yield. Unlike the Aus-tralian situation, barley is the dominant crop in the semiarid and arid areas of WANA. Since crops in dry areas are more prone to be aff ected by BT, barley probably is the crop most

frequently aff ected by BT in WANA, thus is an appropriate crop for studying BT.

SalinityBoron is often found in high concentrations in associa-tion with salinity problems (Keren and Bingham, 1985; Holloway and Alston, 1992; Adcock et al., 2007). So far, contrasting results have been reported on the B by salin-ity interaction eff ects. A negative interaction was detected by Holloway and Alston (1992). Surprisingly, increasing salinity decreased stem-B concentrations and reduced shoot death by 80% at the highest B level in a study on Prunus rootstocks (El-Motaium et al., 1994). Sulfate could be responsible for the salinity-induced decline in tissue-B concentrations, but the authors (El-Motaium et al., 1994) could not give any reason for this interaction. Results of this rootstock study supported an earlier report on linseed (Linum usitatissimum L.) (Chauhan et al., 1984), but were diff erent from that reported on a wheat experiment by Bingham et al. (1987), in which the B by salinity interac-tion was not signifi cant for shoot dry weight and leaf-B concentration. The use of a mixture of Cl with SO

4 instead

of just Cl by El-Motaium et al. (1994) and Chauhan et al. (1984) might have caused the diff erence in results between their studies and that of Bingham et al. (1987).

Figure 2. Different severity of B-toxicity symptoms on barley leaves

from nine varieties.


Nutrients

Low Zn levels, but high B levels, are found in some alkaline soils in semiarid areas, for example, in the Central Anato-lian Plateau of Turkey (Çakmak et al., 1996). Zinc defi -ciency was reported to increase B accumulation in barley to a toxic level (Graham et al., 1987), with the indication that Zn performs a protective role at the root surface. Later, it was further shown that the role of Zn in reducing tissue-B concentrations is not only due to increased growth of wheat plants (Singh et al., 1990). Using sour orange (Citrus xauran-tium L.) seedlings, Swietlik (1995) showed that there was a signifi cant B by Zn interaction on shoot growth, leaf and stem dry weight, and leaf area, suggesting that the eff ects of B were modifi ed by Zn nutrition. Zinc-defi cient seedlings developed more BT symptoms than Zn-suffi cient seedlings, and suff ered growth reduction. This fi nding has potential practical application since BT could be mitigated with Zn application. However, a study in a Zn-defi cient and B-toxic fi eld in Turkey did not fi nd that Zn fertilization infl uenced B concentration (Torun et al., 2001), but for many cultivars there was a close relationship between tolerance to Zn defi -ciency and to BT.

Studies of B by N interaction have been performed since the 1950s (Salinas et al., 1987), but results have been inconsistent. Addition of 50 mg kg–1 N or more to the soil reduced B uptake and alleviated BT in barley and wheat under glasshouse conditions (Gupta et al., 1976), but not under fi eld conditions. When B levels in nutrient solution were yield-limiting, higher rates of N applications did not prevent BT on pea in the glasshouse study by Salinas et al. (1987), but application of N markedly increased leaf, stem, and root dry weights and generally reduced the B concen-trations in leaves and stems of pistachio (Pistacia vera L.) seedlings (Sepaskhah and Maftoun, 1994). Using glasshouse pot experiments, Salinas et al. (1986) showed that the toxic eff ects of B on pod yield of pea was reduced by the addition of Mg at higher than normal rates, and Sotiropoulos et al. (1999) showed that the presence of Ca at 12 mM in nutri-ent solutions signifi cantly decreased B levels in kiwifruit plants and alleviated BT. With the exception of Gupta et al. (1976), these studies were conducted in pots under glass-house conditions. Clearly, results need to be followed up in fi eld experiments, and the economics of applying above-normal rate of N or Mg needs to be assessed.

BREEDING FOR BORON-TOXICITY TOLERANCEIt is neither practical nor easy to detoxify high B soil by agronomic means (Leyshon and Jame, 1993). One may leach the soil extensively by using much more water than what is needed to remove soluble salt. However, since B is removed more slowly than salinity during leaching, it may still be excessive in some reclaimed soils (Bingham et al., 1987), and availability of water in dry areas always

is an insurmountable constraint. The use of triisopropa-nolamine (1,1′,1″-nitrilo-tri-2-propanol) to incorporate B into a complex organic molecule harmless to plants was tested by Hutchinson and Viets (1969), but they pointed out that its use for B detoxifi cation in practical agriculture would not be economical and might not work under fi eld conditions. In addition, lime application to increase pH and B adsorption by soil is not suitable for alkaline soils.

Selecting or breeding crop cultivars with high BT tol-erance is the only practical approach to increase or main-tain yields on high-B soils. As the highest concentrations of B occur in the subsoil, improving BT tolerance not only will increase yield in high-B soil because of resis-tance or tolerance to BT per se, but BT-tolerant plants may exploit the subsoil with roots to use the water reserve, which can be of major benefi t in years of drought (Hol-loway and Alston, 1992). Yau (2002b) demonstrated that BT tolerance as well as drought tolerance are needed in dry areas having high levels of subsoil B.

Phenotypic VariationBefore starting a breeding program to improve BT tolerance, sources of BT tolerance must exist. Extensive surveys on ger-mplasm in diff erent crop species have been performed (Nable et al., 1997). Table 2 lists some of the BT-tolerant lines or cul-tivars for diff erent fi eld crop species. Commonly, tolerance implies little or no BT symptoms, low tissue B concentra-tions, and good growth or yield under high soil-B. How-ever, using the above criteria, earlier studies in durum wheat (Yau et al., 1995c, 1997a) were not able to detect cultivars, lines, or accessions that are really BT tolerant. Later, Yau et al. (1997b) showed that some durum lines yield as well as the BT-tolerant bread wheat check in high-B soil and do not suf-fer yield reduction relative to the low-B soil, although having higher BT symptom scores and tissue B concentrations. Yau et al. (1997b) suggested that durum wheat may use a diff er-ent strategy to adapt to high-B soil; for example, localizing B in the leaf tips, so one should not directly compare durum wheat with bread wheat on symptom severity and tissue-B concentration. Similar results were obtained in a study con-ducted in Turkey where the authors claim that the internal mechanisms (e.g., adsorption to cell walls and compartmen-tation of B in vacuoles) could be a more plausible explanation for B tolerance in durum wheat (Torun et al., 2006).

In genetic studies on variation in response to BT on a range of crops, for example, bread wheat (Paull et al., 1991), barley ( Jenkin and Lance, 1991), peas (Bagheri et al., 1992), medics (Medicago spp.) (Paull et al., 1992), and durum wheat ( Jamjod et al., 1994), BT tolerance was shown to be under the control of major additive genes (Nable et al., 1997). In bread wheat, chromosomes of homoeologous groups 4 and 7 were implicated in the control of BT tol-erance, and analysis of single chromosome recombinant lines identifi ed that one gene is on 4AL and linked to Sr 7a


(Paull et al., 1993). Using monosomic analysis, BT toler-ance of ‘Halberd’ is controlled by a gene in chromosome 7B (Chantachume et al., 1993).

Progress in BreedingBreeding to incorporate BT tolerance has been met with diff erent degrees of success in Australia, where wheat breeders have been successful in breeding new bread wheat cultivars with good tolerance, for example, ‘Frame’, ‘Krichauff ’, and ‘Yitpi’ (Eglinton et al., 2004). The source of BT tolerance could be traced back to ‘Federation’ via Halberd and ‘Insignia’, two dominant old Australian cul-tivars. Breeding for BT tolerance by backcrossing has been relatively easy in bread wheat since only a few additive genes are involved in BT tolerance in bread wheat (Paull et al., 1991). The BT-tolerance gene ‘Bo1’ was transferred from Halberd to ‘BT-Schomburgk’, making it yield bet-ter than the recurrent parent ‘Schomburgk’ on high-B soils (Rathjen et al., 1995). The latest study conducted in northwestern Victoria testing three bread wheat cultivars with BT tolerance over a range of soil B and salinity levels commonly existing in fi elds showed that the cultivars had relatively greater tolerance to BT than to salinity (Nut-tall et al., 2006). The authors (Nuttall et al., 2006) sug-gested that future cultivars would need to have higher salinity tolerance as well. Australian farmers started grow-ing durum wheat only recently, and unlike bread wheat durum breeding was a relatively new endeavor. The BT-tolerant line WD99006 bred by Tony Rathjen has been released (Cooper, 2004).

In breeding for BT tolerance in barley at the Waite Institute of the University of Adelaide in South Australia, a tall, six-row African landrace, ‘Sahara’, was used as the source of tolerance and crossed with two nontolerant lines (an Australian cultivar and a breeder’s line from neighbor-ing Victoria). Two BT-tolerant genes from Sahara were

the targets of transfer to the off spring. However, reported results were disappointing up to 2002. Although the back-cross lines displayed less BT symptoms than the non–BT-tolerant parents, they did not yield more than the parents (McDonald et al., 2002).

This unsuccessful attempt to improve yield by upgrad-ing BT tolerance was attributed to two causes. First, Sahara is a low-yielding line and has many poor agro-nomic characteristics. Genes from Sahara unrelated to tol-erance might also have been transferred, thus limiting the yield of the BT-tolerant lines. Second, the very dry spring in 2002 might mean that most of the subsoil moisture reserves were used before anthesis and did not make much contribution to grain-fi lling (McDonald et al., 2002).

The latest information on success in breeding barley and lentil lines or cultivars with BT tolerance was obtained from the Grain Research Development Corporation (GRDC) website (http://www.grdc.com.au). The new malting barley cultivar Sloop Vic, which has some BT tol-erance from Sahara, had up to a 10% yield advantage over the non–BT-tolerant ‘Sloop’ on high B soils in Victoria. Besides, the advanced feed barley line, WI3804, which had a good chance of being released, was well adapted to high-B soils and water-stressed conditions.

Eff orts to improve the tolerance to BT and salinity have also been spent on lentil. Information obtained from the GRDC website indicated that a line designated as 02-355L*03HS005, which has combined salt and BT tol-erance, out-yielded ‘Nugget’, which is currently the most widely grown cultivar in areas having BT and salt prob-lems, by 100%.

Breeding for BT tolerance in Australia showed easier success in bread wheat than in other species, due to the fact that old cultivars with BT tolerance and adapted to Australian conditions existed in bread wheat. For barley, durum wheat, and lentil, foreign germplasm not adapted

Table 2. Best boron-toxicity tolerant lines or cultivars (origin in parentheses) in different fi eld crop species.

Crop Name of line, cultivar (origin) Reference

Barley Sahara 3763 (Algeria) Nable (1988)

Baluchistan (Pakistan), ICB 104041 (Afghanistan), Tadmor (Syria), Tokak (Turkey), Walfajr (Iran) Yau (1997)

Durum wheat Candeal de Grao Escuro no. 7746, Senatore Cappelli (Italy) Yau et al. (1997b)

ICDW 7674 (Afghanistan) Yau (1997)

Bread wheat Halberd (Australia), (Wq*KP)*WmH/6/12 (Australia) Paull et al. (1988)

Greek ( = G6140; Greece) Nable (1988)

India 126 (India), Benventuto Inca (Argentina), Turkey 1473 (Turkey), Abyssinia 10 (Ethiopia), Iraq 22

(Iraq), Klein Granador (Argentina), Lin Calel (Argentina)

Chantachume et al. (1995)

Shi#4414/Crow’S’ (ICARDA, Syria) Yau (1997)

Lentil ILL 5883 (ICARDA, Syria), ILL 1765 (Afghanistan) Yau and Erskine (2000)

ILL 2024, ILL 0213A Hobson et al. (2006)

Pea SA 132 and SA 310 (Afghanistan) Bagheri et al. (1994)

Medics Cyprus Paull et al. (1992)

Brassica rapa WWY Sarson (Australia), Local (India) Kaur et al. (2006)

Rice IR42, IR46, IR48, IR54, and IR9884-54 (IRRI, the Philippines) Dobermann and Fairhurst (2000)


to Australia has to be used as donor parents, and it will take time to remove the unrelated but poor-yielding genes.

Unlike Australian conditions, improvement of BT tolerance in barley was obtained fairly easily by ICARDA in Syria. In fact, no eff orts had been spent on direct selec-tion for tolerance. Breeding for drought tolerance through pure line selection of landraces at two arid sites (Breda and Boueider) with high subsoil-B levels yielded productive lines with good tolerance to BT, for example, SLB 5-96, Zanbaka, SLB 39-60, and Tadmor (Yau et al., 1994a). This success supports the concept raised in Australia that BT tolerance is needed for drought tolerance in dry areas with high-B subsoil.

Similar to barley breeding in ICARDA, breeding for drought tolerance in lentil through pure line selection of landraces at Breda yielded productive lines with good BT tolerance. A good example is ILL5883, which was the most BT-tolerant line in 2000, and was selected for pos-sible release in Iraq and Syria (Yau and Erskine, 2000).

Relative to barley, less eff ort has been placed on improving BT tolerance in wheat in WANA, largely because barley cultivation dominates in arid and semiarid areas while wheat is mainly grown in moderate rainfall areas or under irrigation. Thus, BT is not a major prob-lem faced by bread wheat. As with barley breeding in ICARDA, BT tolerance in wheat was obtained through testing and selection of materials at Breda. Entries having lower BT symptoms and tissue B concentrations than Hal-berd, the BT-tolerant Australian check, were found in a screening in the glasshouse (Yau et al., 1994b). Regarding durum wheat, the best lines had symptom scores as low as Halberd or had a lower reduction in grain yield in a high-B soil, but none had B concentrations as low as Halberd (Yau et al., 1994b, 1995b). A suggestion that durum wheat could tolerate higher tissue B concentration than bread wheat was put forward (Yau et al., 1994b).

CONCLUSIONSNatural selection has been so successful that the problem of high soil B escaped detection for a long time in dry areas of the world such as the Mediterranean and Austra-lia. As more emphasis is being placed on development of dryland farming, and as the various nutrient constraints are being identifi ed and dealt with, and as new high-yield potential varieties are being developed, BT will inevitably emerge as a crop production constraint. However, unlike other nutrient defi ciencies that can be rectifi ed by fertil-izer application, or other micronutrient toxicity such as Mn, which can be controlled by liming, BT is unique in that it is in practice not amenable to soil intervention.

It is clear from this review of BT that we need to adopt the more practical approach of modifying the plants to adapt to the soil instead of continuing to use the expen-sive orthodox approach of modifying the soil to fi t the

plants. Nature has chosen the former approach as many of the landraces from dry areas in WANA have good BT tolerance that can be exploited by plant breeders to pro-duce modern crop varieties that incorporate the tolerance genes as well as other desirable yield related traits. Unlike salinity, the use of BT-tolerant varieties will not lead to a buildup of B or lead to crop failure in rainfed areas. In irrigated areas where soil B accumulates due to the use of high-B water, the availability of BT-tolerant varieties will give researchers and administrators a longer period to search for the best strategy for farmers to adopt. We believe that this brief review can contribute to bringing the phenomenon of BT to the attention of researchers and ultimately raise the ceiling of crop production at the global level, particularly in the world’s drylands.

AcknowledgmentsWe thank Mustafa Pala, Cropping Systems Agronomist,

ICARDA, for reviewing the manuscript.

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