HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Yau, S. K. Articles by Ryan, J. Search for Related Content PubMed Articles by Yau, S. K. Articles by Ryan, J. Agricola Articles by Yau, S. K. Articles by Ryan, J. Related Collections Nutrient Management Plant Genetic Resources Crop Ecology

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

^a Faculty of Agricultural and Food Sciences, American Univ. of Beirut, P.O. Box 11-0236, Beirut, Lebanon
^b International Center for Agricultural Research in the Dry Areas (ICARDA), P.O. Box 5466, Aleppo, Syria

^* Corresponding author (sy00{at}aub.edu.lb).

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
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 Australia. 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 tolerance. The importance of BT was not adequately recognized until the 1980s, when scientists discovered that BT caused significant crop yield reductions in South Australia. We offer several 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 field, BT in crops usually is more prominent after drought, indicating that both BT and drought tolerance are needed in crops for dry areas having 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 surveys 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.

Abbreviations: BT, boron toxicity • ICARDA, International Center for Agricultural Research in the Dry Areas • WANA, West Asia and North Africa

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
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 symptoms 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 different amounts of boric acid were added, that I was finally convinced that the symptoms we had observed were indeed BT.

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
Research in soil fertility, plant nutrition, and plant breeding has identified and largely eliminated nutrient constraints, especially in the developed world. Besides, the supply and efficient use of fertilizers have been enhanced, and the yield potential of varieties to better nutrition has been raised. The predominant emphasis of soil and agronomic research has been on rectifying nutrient deficiencies in an economically and environmentally benign manner. Efforts 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 deficiency. This dichotomy is well illustrated in the case of B, whose deficiency and the implications for crop production 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, reflecting 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 deficiency is a widespread problem in relatively humid areas of the world (Gupta, 1979). Some early surveys (Berger, 1962) have shown that deficiency 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 deficiency; 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 reflected the accumulating knowledge on B deficiency and its wider implications.

Relative to B deficiency, 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 deficiency and toxicity is narrow (Mortvedt et al., 1991). Despite the fact that one of the first 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 unappreciated by soil and crop scientists—and ignored in the literature. For instance, only a fleeting reference, without 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 significant yield reduction in common wheat (Triticum aestivum L.) attributed to excess B; others (Yau and Saxena, 1997; Yau et al., 1996) confirmed 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 problem 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 interested 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). Earlier reviews by Gupta et al. (1985) and Gupta (1993a) have concentrated on soil and environmental factors related to B. This article reflects our combined experience in both Australia and the Mediterranean region, where the problem of BT is endemic. The review by a plant breeder and a soil scientist reflects a paradigm shift from soil amelioration to breeding for crop tolerance.

	BRIEF HISTORICAL ACCOUNT ON BORON TOXICITY

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
Boron toxicity in field crops was probably first 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 efforts 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 profile, 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 profile depth are illustrated (Fig. 1 ) for ICARDA's driest site for barley testing (Boueider) in Syria. Eight out of the 10 profiles show that B concentrations increase substantially from 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 conspicuous 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 comparing WANA with Western Europe, where B deficiency is common.
   
5. The fact that phloem mobility of B varies dramatically with species (e.g., cereals vs. some fruit trees) and causes profoundly different BT symptoms could have confused earlier workers. This point will be further discussed later.
   

View larger version (10K): [in this window] [in a new window]   Figure 1. Patterns of depthwise distribution of water soluble B from 10 profiles at Boueider, a dry site in northern Syria (Ryan et al., 1998).

	AREAS WITH NATURALLY OCCURRING HIGH-BORON SOILS

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

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 deficiency (Gupta and Gupta, 1998), application or disposal of fossil combustion residues such as coal fly 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 different geographic 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 significant findings on B mobility (Brown and Hu, 1996), came from California. High-B soils are also found in the Lower Rio Grande Valley of Texas, where there are high indigenous B levels and where well water also contains high B levels (Cooper et al., 1955).

Probably the country of greatest significance 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 concentrations (CaCl₂ 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 Australia, 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), deficient 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 increasing 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 CaCO₃ and clay content, together with the dry weather, enhance B fixation (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 identified recently in Turkey (Torun et al., 2003). Based on a survey on BT symptoms in barley crops, Avci and Akar (2005) claimed that BT is not a widespread problem in the Central Anatolia and Transitional 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 (Rhodoxeralf) soils contains above-average level of water-soluble B (>3.0 mg kg^–1) (Ravikovitch et al., 1961). Besides the southwestern 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 (Chauhan and Asthana, 1981). Underground water for irrigation 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 northern 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 Philippines (Dobermann and Fairhurst, 2000). Besides wells, water from creeks flowing through outcrops of borate deposits was found to contain high levels of B in southern California (Kelley and Brown, 1929).

Based on Toxicity Symptoms
Boron toxicity symptoms were identified, 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 Turkey, BT symptoms were detected in farmers' fields 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 suggested 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 barley 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-fifth of the 50 Iraqi accessions were BT tolerant, and the tolerant accession ‘ICB 104041’ from Afghanistan had significantly 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.

View this table: [in this window] [in a new window]   Table 1. Boron-toxicity symptom scores and dry weight change in B25 for two contrasting groups of winter or facultative barley in the Barley High Elevation Adaptation Yield Trial (Yau, 2002a).

	PHLOEM MOBILITY OF BORON

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
The 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 field 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.

View larger version (96K): [in this window] [in a new window]   Figure 2. Different severity of B-toxicity symptoms on barley leaves from nine varieties.

This different 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 affinity 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 meristemic 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 granatum 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 differences in B phloem mobility and expression of BT symptoms has significance for the diagnosis 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 tissues is needed. In California, for almonds, there is a widespread 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

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
Drought
That high B levels usually occur in subsoil explains why the problem of BT was usually discovered after a drought (Cartwright et al., 1986). According to Adcock et al. (2007), subsoil 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 effect than salt in reducing wheat root density with depth; at a high B level, few roots penetrated below 0.4 m. Associated with this decrease in root density with depth, soil water increased in the lower part of the profile. This led Holloway and Alston (1992) to conclude 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 deleterious effects of B and salt on root growth may prevent subsoil moisture from being used.

Since drought has such a big effect on BT, our group expanded the research. In the preliminary study, there was no interaction between the effects of terminal drought and BT on barley grain yield and many other agronomic characters (Yau, 2001). As drought may occur at different growth stages, and there are differences among varieties in BT tolerance, the next study involved early, midseason, 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 experiment, significant B by drought interaction was detected with root growth in the subsoil, straw B concentration, and straw and biological yields for the BT-susceptible genotype, 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. Depending 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 different growth stages, B was top-dressed; creating an artificial situation that was different from the field conditions. To mimic the field situation better, tubes were split into half horizontally to study the effects 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 (joining the bottom section to the top section) on the development, 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 effects of B on crops in the fields, but high subsoil B levels can cause yield reduction even when roots reach it as late as the boot stage. This finding was supported by field 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 Australian situation, barley is the dominant crop in the semiarid and arid areas of WANA. Since crops in dry areas are more prone to be affected by BT, barley probably is the crop most frequently affected by BT in WANA, thus is an appropriate crop for studying BT.

Salinity
Boron is often found in high concentrations in association 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 salinity interaction effects. 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 different from that reported on a wheat experiment by Bingham et al. (1987), in which the B by salinity interaction was not significant for shoot dry weight and leaf-B concentration. The use of a mixture of Cl with SO₄ instead of just Cl by El-Motaium et al. (1994) and Chauhan et al. (1984) might have caused the difference in results between their studies and that of Bingham et al. (1987).

Nutrients
Low Zn levels, but high B levels, are found in some alkaline soils in semiarid areas, for example, in the Central Anatolian Plateau of Turkey (Çakmak et al., 1996). Zinc deficiency 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 xaurantium L.) seedlings, Swietlik (1995) showed that there was a significant B by Zn interaction on shoot growth, leaf and stem dry weight, and leaf area, suggesting that the effects of B were modified by Zn nutrition. Zinc-deficient seedlings developed more BT symptoms than Zn-sufficient seedlings, and suffered growth reduction. This finding has potential practical application since BT could be mitigated with Zn application. However, a study in a Zn-deficient and B-toxic field in Turkey did not find that Zn fertilization influenced B concentration (Torun et al., 2001), but for many cultivars there was a close relationship between tolerance to Zn deficiency 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 field 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 concentrations 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 effects 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 nutrient solutions significantly decreased B levels in kiwifruit plants and alleviated BT. With the exception of Gupta et al. (1976), these studies were conducted in pots under glasshouse conditions. Clearly, results need to be followed up in field experiments, and the economics of applying above-normal rate of N or Mg needs to be assessed.

	BREEDING FOR BORON-TOXICITY TOLERANCE

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
It 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 triisopropanolamine (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 detoxification in practical agriculture would not be economical and might not work under field 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 tolerance is the only practical approach to increase or maintain 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 resistance 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 benefit in years of drought (Holloway 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 Variation
Before starting a breeding program to improve BT tolerance, sources of BT tolerance must exist. Extensive surveys on germplasm in different crop species have been performed (Nable et al., 1997). Table 2 lists some of the BT-tolerant lines or cultivars for different field crop species. Commonly, tolerance implies little or no BT symptoms, low tissue B concentrations, and good growth or yield under high soil-B. However, 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 suffer 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 different 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 conducted in Turkey where the authors claim that the internal mechanisms (e.g., adsorption to cell walls and compartmentation of B in vacuoles) could be a more plausible explanation for B tolerance in durum wheat (Torun et al., 2006).

Progress in Breeding
Breeding to incorporate BT tolerance has been met with different 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 cultivars. 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 better 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 fields showed that the cultivars had relatively greater tolerance to BT than to salinity (Nuttall et al., 2006). The authors (Nuttall et al., 2006) suggested that future cultivars would need to have higher salinity tolerance as well. Australian farmers started growing 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 neighboring Victoria). Two BT-tolerant genes from Sahara were the targets of transfer to the offspring. However, reported results were disappointing up to 2002. Although the backcross 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 upgrading BT tolerance was attributed to two causes. First, Sahara is a low-yielding line and has many poor agronomic characteristics. Genes from Sahara unrelated to tolerance 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-filling (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 tolerance 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.

Efforts 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 tolerance, out-yielded ‘Nugget’, which is currently the most widely grown cultivar in areas having BT and salt problems, 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 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 efforts had been spent on direct selection 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 possible release in Iraq and Syria (Yau and Erskine, 2000).

Relative to barley, less effort 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 problem 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 Halberd, 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).

	CONCLUSIONS

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
Natural 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 Australia. As more emphasis is being placed on development of dryland farming, and as the various nutrient constraints are being identified 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 deficiencies that can be rectified by fertilizer 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 expensive orthodox approach of modifying the soil to fit 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 produce 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.

	ACKNOWLEDGMENTS

 
We thank Mustafa Pala, Cropping Systems Agronomist, ICARDA, for reviewing the manuscript.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.

Received for publication October 1, 2007.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION INTRODUCTION BRIEF HISTORICAL ACCOUNT ON... AREAS WITH NATURALLY OCCURRING... PHLOEM MOBILITY OF BORON INTERACTION OF BORON TOXICITY... BREEDING FOR BORON-TOXICITY... CONCLUSIONS REFERENCES

 

• Adcock, D., A.M. McNeill, G.K. McDonald, and R.D. Armstrong. 2007. Subsoil constraints to crop production on neutral and alkaline soils in south-eastern Australia: A review of current knowledge and management strategies. Aust. J. Expt. Agric. 47:1245–1261.[CrossRef]
• Al-Khafaji, A. 1995. Boron in soil and water in Iraq. p. 204–208. In J. Ryan (ed.) Accomplishments and future research in dryland soil fertility research in the Mediterranean area. ICARDA, Aleppo, Syria.
• Amadi, T.H., and I.T. Lazim. 1989. A study on micronutrients distribution in northern Iraqi soils. Zanco 2:19–37.
• Ashworth, L.J., Jr., S.A. Gaona, and E. Surber. 1985. Nutritional diseases of pistachio trees: Potassium and phosphorus deficiencies and chloride and boron toxicities. Phytopathology 75:1084–1091.[Web of Science]
• Avci, M., and T. Akar. 2005. Severity and spatial distribution of boron toxicity in barley cultivated areas of Central Anatolia and Transitional Zones. Turk. J. Agric. For. 29:377–382.
• Bagheri, A., J.G. Paull, and A.J. Rathjen. 1994. The response of Pisum sativum L. germplasm to high concentrations of soil boron. Euphytica 75:9–17.[CrossRef][Web of Science]
• Bagheri, A., J.G. Paull, A.J. Rathjen, S.M. Ali, and D.B. Moody. 1992. Genetic variation in the response of pea (Pisum sativum L.) to high soil concentrations of boron. Plant Soil 146:261–269.[CrossRef][Web of Science]
• Berger, K.C. 1962. Micronutrient deficiencies in the United States. J. Agric. Food Chem. 10:178–181.[CrossRef][Web of Science]
• Bingham, F.T., J.E. Strong, J.D. Rhoades, and R. Keren. 1987. Effects of salinity and varying boron concentrations on boron uptake and growth of wheat. Plant Soil 97:345–351.[CrossRef][Web of Science]
• Bradford, G.R. 1966. Boron. p. 33–61. In H.D. Chapman (ed.) Diagnostic criteria for plants and soils. University of California, Riverside, CA.
• Brady, N.C., and R.R. Weil. 1999. The nature and property of soils. 12th ed. Prentice Hall, Upper Saddle River, NJ.
• Branson, R.L. 1976. Soluble salts, exchangeable sodium and boron in soil. p. 42–45. In H.M. Reisenauer (ed.) Soil and plant-tissue testing in California. Division of Agric. Sci., Univ. of Calif. Ext. Bull. 1879.
• Brennan, R.F., and K.G. Adcock. 2004. Incidence of boron toxicity in spring barley in southwestern Australia. J. Plant Nutr. 27:411–425.[CrossRef][Web of Science]
• Brown, P.H., and H. Hu. 1996. Phloem mobility of boron is species dependent: Evidence for phloem mobility in sorbitol-rich species. Ann. Bot. (Lond.) 77:497–505.[Abstract/Free Full Text]
• Brown, P.H., and H. Hu. 1998a. Phloem boron mobility in diverse plant species. Bot. Acta 111:331–335.[Web of Science]
• Brown, P.H., and H. Hu. 1998b. Boron mobility and consequent management in different crops. Better Crops Plant Food 82:28–31.
• Brown, P.H., H. Hu, and W.G. Roberts. 1999. Occurrence of sugar alcohols determines boron toxicity symptoms of ornamental species. J. Am. Soc. Hortic. Sci. 124:347–352.
• Çakmak, I., A. Yilmaz, M. Kalayci, H. Ekiz, A.C. lger, and H.J. Braun. 1996. Zinc deficiency and boron toxicity as critical nutritional problems in wheat production in Turkey. p. 279. In Proc. 5th International Wheat Conference, Ankara, Turkey. 10–14 June 1996.
• Cartwright, B., B.A. Zarcinas, and A.H. Mayfield. 1984. Toxic concentrations of boron in a red-brown earth at Gladstone, South Australia. Aust. J. Soil Res. 22:321–332.
• Cartwright, B., B.A. Zarcinas, and L.R. Spoucer. 1986. Boron toxicity in south Australian barley crops. Aust. J. Agric. Res. 37:351–359.[CrossRef][Web of Science]
• Chantachume, Y., A.J. Rathjen, J.G. Paull, and K.W. Shepherd. 1993. Genetic studies on boron tolerance of wheat. p. 74–75. In B.C. Imrie and J.B. Hacker (ed.) Proc. Tenth Australian Plant Breeding Conf., Vol. 2., Gold Coast, QLD. 18–23 Apr. 1993. Organizing Committee, Australian Convention and Travel Service, Canberra, Australia.
• Chantachume, Y., D. Smith, G.J. Hollamby, J.G. Paull, and A.J. Rathjen. 1995. Screening for boron tolerance in wheat (T. aestivum) by solution culture in filter paper. Plant Soil 177:249–254.[CrossRef][Web of Science]
• Chauhan, R.P.S., and A.K. Asthana. 1981. Tolerance of lentil, barley and oats to boron in irrigation water. J. Agric. Sci. 97:75–78.
• Chauhan, R.P.S., C.P.S. Chauhan, and S.K. Chauhan. 1984. Effect of boronated saline irrigation water on linseed. J. Agric. Sci. 102:237–240.
• Choe, J.S., J.C. Lee, S.B. Kim, and J.Y. Moon. 1986. Studies on the cause of shoot die-back in pear trees (Pyrus serotina Rehder). J. Korean Soc. Hortic. Sci. 27:149–156.
• Christensen, J.J. 1934. Nonparasitic leaf spots of barley. Phytopathology 24:726–742.[Web of Science]
• Cooper, D. 2004. Improving durum wheat production on soils affected by transient salinity. Available at www.grdc.com.au/director/events/researchupdates.cfm?item_id=AC8FF1C3D0260DDC67CCAB846B9DC8E5&pageNumber=65 (verified 11 Mar. 2008). Australian Government, Grains Research and Development Corp, Barton, ACT.
• Cooper, W.C., A. Peynado, and A. Shull. 1955. Boron accumulation in citrus as influenced by rootstock. J. Rio Grande Valley Hortic. Sci. 9:86–94.
• Dobermann, A., and T. Fairhurst. 2000. Rice. Nutrient disorders & nutrient management. handbook series. Potash & Phosphate Institute, Atlanta, GA, Potash & Phosphate Institute of Canada, and International Rice Research Institute, Los Banos, the Philippines.
• Eaton, F.M. 1935. Boron in soils and irrigation waters and its effects on plants with particular reference to the San Joaquin Valley of California. USDA Tech. Bull. 448.
• Eglinton, J., A. Barr, S. Jefferies, H. Kuchel, and J. Reinheimer. 2004. Plant breeding for the tough times. Available at www.grdc.com.au/director/events/researchupdates.cfm?item_id=AC8FFB18DB2C61FEBB1DA078FF16AAC9&pageNumber=88 (verified 11 Mar. 2008). Australian Government, Grains Research and Development Corp, Barton, ACT.
• El-Motaium, R., H. Hu, and P.H. Brown. 1994. The relative tolerance of six Prunus rootstocks to boron and salinity. J. Am. Soc. Hortic. Sci. 119:1169–1175.
• Elseewi, A.A. 1974. Some observations on boron in water, soils, and plants at various locations in Egypt. Alexandria J. Agric. Res. 22:463–473.
• Graham, R.D., R.M. Welch, D.L. Grunes, E.E. Cary, and W.A. Norvell. 1987. Effect of zinc deficiency on the accumulation of boron and other mineral nutrients in barley. Soil Sci. Soc. Am. J. 51:652–657.[Abstract/Free Full Text]
• Gupta, U.C. 1979. Boron nutrition of crops. Adv. Agron. 31:273–307.
• Gupta, U.C. 1993a. Boron and its role in crop production. In U.C. Gupta (ed.) Boron and its role in crop production. CRC Press, Boca Raton, FL.
• Gupta, U.C. 1993b. Deficiency and toxicity symptoms of boron in plants. In U.C. Gupta (ed.) Boron and its role in crop production. CRC Press, Boca Raton, FL.
• Gupta, U.C., and S.C. Gupta. 1998. Trace element toxicity relationships to crop production and livestock and human health: Implications for management. Commun. Soil Sci. Plant Anal. 29:1491–1522.[Web of Science]
• Gupta, U.C., Y.W. Jame, C.A. Campbell, A.J. Leyshon, and W. Nicholaichuk. 1985. Boron toxicity and deficiency: A review. Can. J. Soil Sci. 65:381–409.
• Gupta, U.C., J.A. MacLeod, and J.D.E. Sterling. 1976. Effects of boron and nitrogen on grain yield and boron and nitrogen concentrations of barley and wheat. Soil Sci. Soc. Am. J. 40:723–726.[Abstract/Free Full Text]
• Hansen, C.J. 1948. Influence of rootstock on injury from excess boron in Frence (Agen) prune and President plum. Proc. Am. Soc. Hortic. Sci. 51:239–244.
• Harmsen, K., and P.L.G. Vlek. 1985. The chemistry of micronutrients in soil. p. 1–42. In P.L.G. Vlek (ed.) Micronutrients in tropical food crop production, Martinus Nijhoff/Dr. W. Junk Publ., Dordrecht, the Netherlands.
• Hobson, K., R. Armstrong, M. Nicolas, D. Connor, and M. Materne. 2006. Response of lentil (Lens culinaris) germplasm to high concentrations of soil boron. Euphytica 151:371–382.[CrossRef][Web of Science]
• Holloway, R.E., and A.M. Alston. 1992. The effects of salt and boron on growth of wheat. Aust. J. Agric. Res. 43:987–1001.[CrossRef][Web of Science]
• Hutchinson, G.L., and F.G. Viets, Jr. 1969. Detoxification of boron in plants with triisopropanolamine. Soil Sci. 108:217–221.
• Jamjod, S., J.G. Paull, and A.J. Rathjen. 1994. Chromosomal location of a gene for boron tolerance in durum wheat (Triticum turgidum L. var durum). p. 225–228. In J. Paull et al. Proceedings, 7th Assembly Wheat Breeding Society of Australia. 25–30 Sept. 1994. Univ. Adelaide, Australia.
• Jenkin, M.J., and R.C.M. Lance. 1991. Genetic studies on boron tolerance in barley. p. 556–557. In L. Munck (ed.) Barley genetics VI. Vol. 1. Short papers. Proc. Sixth Int. Barley Genetics Symp., Helsingborg, Sweden. 22–27 July 1991.
• Kaur, S., M.E. Nicolas, R. Ford, R. Norton, and P.W.J. Taylor. 2006. Selection of Brassica rapa genotypes for tolerance to boron toxicity. Plant Soil 285:115–123.[CrossRef][Web of Science]
• Kelley, W.P., and S.M. Brown. 1929. Boron in the soils and irrigation waters of southern California, and its relation to citrus and walnut culture. Hilgardia 3:445–458.
• Keren, R., and F.T. Bingham. 1985. Boron in water, soils, and plants. Adv. Soil Sci. 1:229–276.
• Khan, Z.D., J. Ryan, and K.C. Berger. 1979. Available boron in calcareous soils of Lebanon. Agron. J. 71:79–82.
• Leyshon, A.J., and Y.W. Jame. 1993. Boron toxicity and irrigation management. In U.C. Gupta (ed.) Boron and its role in crop production. CRC Press, Boca Raton, FL.
• Li, C.J. (ed.). 2005. Plant nutrition for food security, human health and environmental protection. Tsinghua Univ. Press, Beijing, China.
• Marschner, H. 1986. Mineral nutrition of higher plants. Academic Press, London.
• McDonald, G., J. Eglinton, L. Davis, and A. Barr. 2002. Breeding for boron tolerance in barley. p. 26–27. In Eyre Peninsula Farming Systems 2002 Summary. Primary Industries and Resources, Adelaide, SA, Australia.
• Moody, D.B., A.J. Rathjen, B. Cartwright, J.G. Paull, and J. Lewis. 1988. Genetic diversity and geographical distribution of tolerance to high levels of soil boron. p. 859–865. In T.E. Miller and R.M.D. Koebner (ed.) Proc. 7th Int. Wheat Genetics Symp., Vol. 2., Cambridge, UK. 13–19 July 1988. Inst. Plant Sci. Res., Cambridge, UK.
• Mortvedt, J.J., F.R. Cox, L.M. Shuman, and R.M. Welch. 1991. Micronutrients in agriculture. Second ed. SSSA Book Ser. 4. SSSA, Madison, WI.
• Nable, R.O. 1988. Resistance to boron toxicity amongst several barley and wheat cultivars: A preliminary examination of the resistance mechanism. Plant Soil 112:45–52.[CrossRef][Web of Science]
• Nable, R.O., G.S. Bañuelos, and J.G. Paull. 1997. Boron toxicity. Plant Soil 193:181–198.[CrossRef][Web of Science]
• Nuttall, J.G., R.D. Armstrong, and D.J. Connor. 2006. Early growth of wheat is more sensitive to salinity than boron at levels encountered in alkaline soils of south-eastern Australia. Aust. J. Exp. Agric. 46:1507–1514.[CrossRef]
• Oertli, J.J. 1960. The distribution of normal and toxic amounts of boron in leaves of rough lemon. Agron. J. 52:530–532.[Abstract/Free Full Text]
• Paull, J.G., B. Cartwright, and A.J. Rathjen. 1988. Response of wheat and barley genotypes to toxic concentrations of soil boron. Euphytica 39:137–144.[CrossRef][Web of Science]
• Paull, J.G., R.O. Nable, A.W.H. Lake, M.A. Materne, and A.J. Rathjen. 1992. Response of annual medics (Medicago spp.) and field peas (Pisum sativum) to high concentrations of boron: Genetic variation and mechanism of tolerance. Aust. J. Agric. Res. 43:203–213.[CrossRef][Web of Science]
• Paull, J.G., A.J. Rathjen, and B. Cartwright. 1991. Major gene control of tolerance of bread wheat (Triticum aestivum L.) to high concentrations of soil boron. Euphytica 55:217–228.[CrossRef][Web of Science]
• Paull, J.G., A.J. Rathjen, P. Langridge, and R.A. Mcintosh. 1993. Location of genes controlling boron tolerance of wheat. p. 1065–1069. Proc. 8th Int. Wheat Genetics Symposium, 20–25 July 1993, Beijing. Chinese Agric. Scientech Press, Beijing.
• Rashid, A., E. Rafique, and N. Bughio. 1994. Diagnosing boron deficiency in rapeseed and mustard by plant analysis and soil testing. Commun. Soil Sci. Plant Anal. 25:2883–2897.[Web of Science]
• Rathjen, A.J., D.B. Moody, B. Cartwright, J. Lewis, D. The, G.A. Palmer, S.P. Jefferies, J.W. Chigwidden, C.J. Stone, H. Wallwork, M.J. Kroehn, G.B. Cornish, and J.G. Paull. 1995. Register of Australian winter cereal cultivars: Triticum aestivum ssp. vulgare (bread wheat) cv. BT-Schomburgk. Aust. J. Exp. Agric. 35:673–674.[CrossRef]
• Ravikovitch, S., M. Maggolin, and J. Navrot. 1961. Micronutrients in soils of Israel. Soil Sci. 92:85–89.
• Riley, M.M., and A.D. Robson. 1994. Pattern of supply affects boron toxicity in barley. J. Plant Nutr. 17:1721–1738.[Web of Science]
• Ryan, J., S. Miyamoto, and J.L. Stroehlein. 1977. Relation of solute and sorbed boron to the boron hazard of irrigation water. Plant Soil 47:253–256.[CrossRef][Web of Science]
• Ryan, J., M. Singh, and S.K. Yau. 1998. Spatial variability of soluble boron in Syrian soils. Soil Tillage Res. 45:407–417.[CrossRef]
• Salinas, R., A. Cerda, F.G. Fernández, and M. Caro. 1987. Interactive effect of boron and nitrogen on pea plants. Agrochimica 31:489–499.[Web of Science]
• Salinas, R., A. Cerda, and V. Martinez. 1986. The interactive effects of boron and macronutrients (P, K, Ca and Mg) on pod yield and chemical composition of pea (Pisum sativum). J. Hortic. Sci. 61:323–347.
• Salinas, R., A. Cerda, M. Romero, and M. Caro. 1981. Boron tolerance of pea (Pisum sativum). J. Plant Nutr. 4:205–217.[Web of Science]
• Sepaskhah, A.R., and M. Maftoun. 1994. Seedling growth and chemical composition of two pistachio cultivars as affected by boron and nitrogen application. J. Plant Nutr. 17:155–171.[Web of Science]
• Sillanpaa, M. 1982. Micronutrients and the nutrient status of soils: A global study. FAO, Rome, Italy.
• Singh, J.P., D.J. Dahiya, and R.P. Narwal. 1990. Boron uptake and toxicity in wheat in relation to zinc supply. Fert. Res. 24:105–110.[CrossRef]
• Sotiropoulos, T. 1997. Boron toxicity of kiwifruit orchards in northern Greece. Acta Hortic. 444:243–247.
• Sotiropoulos, T.E., I.N. Therios, and K.N. Dimassi. 1999. Calcium application as a means to improve tolerance of kiwifruit (Actinidia deliciosa L.) to boron toxicity. Scientia Hortic. 81:443–449.[CrossRef]
• Swietlik, D. 1995. Interaction between zinc deficiency and boron toxicity on growth and mineral nutrition of sour orange seedlings. J. Plant Nutr. 18:1191–1207.[Web of Science]
• Torun, A., I. Gültekin, M. Kalayci, A. Yilmaz, S. Eker, and I. Cakmak. 2001. Effects of zinc fertilization on grain yield and shoot concentrations of zinc, boron, and phosphorus of 25 wheat cultivars grown on a zinc-deficient and boron-toxic soil. J. Plant Nutr. 24:1817–1829.[CrossRef][Web of Science]
• Torun, A., I. Gültekin, M. Kalayci, A. Yilmaz, S. Eker, I. Cakmak, B. Torun, M. Kalayci, L. Ozturk, A. Torun, M. Aydin, and I. Cakmak. 2003. Differences in shoot boron concentrations, leaf symptoms, and yield of Turkish barley cultivars grown on boron-toxic soil in field. J. Plant Nutr. 26:1735–1747.[CrossRef][Web of Science]
• Torun, A.A., A. Yazici, H. Erdem, and I. Cakmak. 2006. Genotypic variation in tolerance to boron toxicity in 70 durum wheat genotypes. Turk. J. Agric. For. 30:49–58.
• Wayne, R. 1986. Boron toxicity in southern cereals. Rural Res. 130:25–27.
• Woodbridge, C.G. 1955. The boron requirement of stone fruit trees. Can. J. Agric. Sci. 35:282–286.
• Yau, S.K. 1997. Differential responses of barley, durum and bread wheat to high levels of soil boron. p. 208–216. In J. Ryan (ed.) Accomplishments and future challenges in dryland soil fertility research in the Mediterranean area. Institut Mondial du Phosphate, Casablanca, Morocco, and ICARDA, Aleppo, Syria.
• Yau, S.K. 2001. Terminal drought and sub-soil boron on barley root growth and water use—An examination of possible interactions. Commun. Soil Sci. Plant Anal. 32:379–387.[CrossRef][Web of Science]
• Yau, S.K. 2002a. European versus West Asian and North African winter barleys in tolerance to boron toxicity. Euphytica 123:307–314.[CrossRef][Web of Science]
• Yau, S.K. 2002b. Interaction of drought, boron-toxicity, and phenotypes on barley root growth, yield, and other agronomic characters. Aust. J. Agric. Res. 53:347–354.[CrossRef][Web of Science]
• Yau, S.K. 2004. Boron toxicity in barley affected by pattern of boron application. p. 59. Abstracts, Int. Symp. on Adaptation of Plants to Water-Limited Mediterranean Environments, Perth, Australia. 20–24 Sept. 2004. CSIRO, Perth, Australia.
• Yau, S.K., S. Ceccarelli, M. Tahir, J. Ryan, M.C. Saxena, and S. Grando. 1995a. Differential responses of barley genotypes to excess soil boron. Barley Newsl. 38:124–127.
• Yau, S.K., and W. Erskine. 2000. Diversity of boron-toxicity tolerance in lentil. Genet. Resour. Crop Evol. 47:55–61.[CrossRef]
• Yau, S.K., J. Hamblin, S. Ceccarelli, M. Tahir, J. Ryan, and S. Grando. 1994a. Screening for boron toxicity resistance. Barley Newsl. 37:110–112.
• Yau, S.K., M. Kalayci, M. Avci, and S.P.S. Beniwal. 1996. Importance of genotypic variation for boron-toxicity tolerance in barley in the Central Anatolian Plateau. Available at wheat.pw.usda.gov/ggpages/BarleyNewsletter/40/Syria_and_Turkey.html. Barley Newsl. 40.
• Yau, S.K., M. Nachit, G. Ortiz-Ferrara, J. Ryan, and M.C. Saxena. 1995b. Differential responses of durum and bread wheat to excess soil boron. Annu. Wheat Newsl. 41:204–207.
• Yau, S.K., M. Nachit, and J. Ryan. 1997a. Variation in growth, development and yield of durum wheat in response to high soil boron. II. Phenotypic differences. Aust. J. Agric. Res. 48:951–957.[CrossRef][Web of Science]
• Yau, S.K., M.M. Nachit, and J. Ryan. 1997b. Variation in boron-toxicity tolerance in a durum wheat core collection. p. 117–120. In R.W. Bell and B. Rerkasem (ed.) Boron in soils and plants. Kluwer Academic Publ., Dordrecht, the Netherlands.
• Yau, S.K., M.M. Nachit, J. Ryan, and J. Hamblin. 1995c. Phenotypic variation of boron-toxicity tolerance in durum wheat at seedling stage. Euphytica 83:185–191.[CrossRef][Web of Science]
• Yau, S.K., M.M. Nachit, J. Ryan, and J. Valkoun. 1998. Boron-toxicity tolerance in durum wheat. p. 174–179. In M.M. Nachit et al. (ed.) SEWANA (South Europe, West Asia and North Africa) Durum Research Network. Proceedings, SEWANA Durum Network Workshop, Aleppo, Syria. 20–23 Mar. 1995. ICARDA, Aleppo, Syria.
• Yau, S.K., J. Ryan, M. Nachit, G. Ortiz-Ferrara, and J. Hamblin. 1994b. Screening for boron toxicity resistance in durum and bread wheat. Annu. Wheat Newsl. 40:204–205.
• Yau, S.K., and M.C. Saxena. 1997. Variation in growth, development and yield of durum wheat in response to high soil boron. I. Boron effects. Aust. J. Agric. Res. 48:945–949.[CrossRef][Web of Science]
• Yau, S.K., and M. Tahir. 1996. Variation in boron-toxicity tolerance causes G x E interaction in yield. p. 138. Abstracts of poster sessions, 2nd Int. Crop Science Congr., New Delhi, India. 17–24 Nov. 1996.

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Yau, S. K. Articles by Ryan, J. Search for Related Content PubMed Articles by Yau, S. K. Articles by Ryan, J. Agricola Articles by Yau, S. K. Articles by Ryan, J. Related Collections Nutrient Management Plant Genetic Resources Crop Ecology