Ecogeographic and evolutionary approaches to improving adaptation of autumn-sown chickpea (Cicer arietinum L.) to terminal drought: The search for reproductive chilling tolerance

Field Crops Research 104 (2007) 112–122 www.elsevier.com/locate/fcr

Ecogeographic and evolutionary approaches to improving adaptation of autumn-sown chickpea (Cicer arietinum L.) to terminal drought: The search for reproductive chilling tolerance J.D. Berger a,b,* b

a CSIRO Plant Industry, Private Bag 5, Wembley, WA 6913, Australia Centre for Legumes in Mediterranean Agriculture, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia

Received 15 December 2006; received in revised form 29 January 2007; accepted 1 March 2007

Abstract Terminal drought is the most important abiotic stress of dryland chickpea. The principal adaptive strategy of the crop is drought escape through early phenology. In regions where average temperatures at flowering <14–16 8C, such as southern Australia or northern South Asia, the lack of reproductive chilling tolerance forces chickpea to delay podset. This delay compromises drought escape by exposing chickpea to terminal drought during much of the pod filling phase, reducing yield potential and stability, depending on seasonal climatic fluctuations. This paper defines chickpea growing seasons in time throughout the crop’s global production regions using published data and feedback from local breeders. This information is used to calculate and map regionally specific chickpea bioclimatic variables such as flowering phase temperatures and the peak rate of growing season temperature change. Flowering phase temperatures <14 8C are uncommon. Mediterranean climates in southern Australia, Chile, California and Portugal tend to be cool during flowering (<15.4 8C), while much of WANA is moderate to warm (15.4–24.4 8C), with exceptions in coastal N Africa, the Nile valley and higher elevations in Morocco, the Balkans, central Afghanistan, NE and SW Iran. Ethiopia contains a wide range of flowering phase temperatures depending on altitude. In South Asia flowering phase temperatures tend to decrease with increasing latitude, with large cool regions in the Punjab, N Haryana, N Uttar Pradesh and the Nepali terai. Superimposing the peak rates of temperature change within the growing season identifies habitats which are likely to be consistently cool throughout the reproductive phase by eliminating regions with transient chilling stress, such as much of N South Asia. It is suggested that reproductive chilling tolerance is rare in chickpea because of the late Neolithic shift from autumn to spring sowing in WANA, and subsequent dissemination into predominantly moderate to warm flowering habitats with only transient low temperature stress. The search for reproductive chilling tolerance should concentrate on these relatively uncommon consistently cool habitats. These are not well represented in the world chickpea collection, a shortcoming which is exacerbated by the lack of passport data in regions of potential interest from Iran to Central Asia. An alternative strategy is to search for reproductive chilling tolerance in the wild Cicer species, which have maintained a winter annual lifecycle and appear to be more cold tolerant than the cultigen. This approach is limited by the lack of germplasm. Currently, there are <30 original wild accessions in the primary genepool of chickpea (C. reticulatum, n = 18; C. echinospermum, n = 10) in the world’s genebanks, so more collection is required. # 2007 Elsevier B.V. All rights reserved. Keywords: Chickpea; Chilling tolerance; Adaptation; Ecogeography; Terminal drought

1. Introduction Chickpea (Cicer arietinum L.) ranks 2nd among the world’s food legumes in terms of area, and is grown principally as a

* Correspondence address: CSIRO Plant Industry, Private Bag 5, Wembley, WA 6009, Australia. Tel.: +61 8 9333 6623; fax: +61 8 9387 8991. E-mail address: [email protected]. 0378-4290/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2007.03.021

cool-season crop in the summer-dominant rainfall systems of South Asia (ca.75% of global production), and as an autumn or spring sown crop in Mediterranean climates in both northern and southern hemispheres (ca. 15% of global production) (FAO, 2006; Berger and Turner, 2007). Rising temperatures in spring/ early summer exposes chickpea to terminal drought stress in both systems, exacerbated by the depletion of stored soil moisture in South Asian regions, and the diminishing withinseason rainfall in Mediterranean areas (Berger and Turner,

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2007). Chickpea sowing strategies attempt to minimize exposure to the key stresses. Thus, South Asian farmers sow early to minimize terminal drought, but are limited by the end of the preceding rainy (kharif) cropping season, and high temperature stress at germination (Berger and Turner, 2007). The traditional farming system of Mediterranean climates in West Asia and North Africa (WANA) exacerbates terminal drought stress because chickpea is sown in early spring to avoid the principal winter stresses of frost, chilling and Ascochyta rabiei disease pressure at the early seedling stage (Walker, 1996). Increased exposure to terminal drought under springsowing decreases season length, delays flowering, reduces dry matter production (Hughes et al., 1987), water use efficiency (Brown et al., 1989), plant height and seed yield (Singh et al., 1997). Adaptation research has confirmed the importance of drought avoidance in chickpea. Although chickpea has a number of characteristics consistent with dehydration postponement and tolerance, such as deep rooting (Saxena et al., 1994), high soil water extraction (Zhang et al., 2000), and osmotic adjustment (Morgan et al., 1991; Lecoeur et al., 1992; Leport et al., 1999; Moinuddin and Khanna-Chopra, 2004; Basu et al., 2007), its primary adaptive strategy to drought stress appears to be escape through early phenology (Silim and Saxena, 1993a,b; Siddique et al., 2001; Berger et al., 2004, 2006). This is underlined by recent work, which has demonstrated that chickpea’s capacity to osmotically adjust did not enhance its productivity under terminal drought (Basu et al., 2007; Turner et al., 2007). Additionally, genotype by environment studies have demonstrated that not only is early phenology an advantage under severe terminal drought, but that early flowering germplasm with high harvest is consistently higher yielding across Mediterranean Australia than later material (Berger et al., 2004). However, the capacity of chickpea to escape terminal drought through early phenology is often compromised by a lack of reproductive chilling tolerance in the crop. When average temperatures at flowering fall below 14–16 8C, chickpea delays the formation of pods, and commences a repeated cycle of flowering and subsequent abortion until temperatures increase (Berger et al., 2004, 2005). This delay exposes chickpea to terminal drought during the critical seed filling stage. In Australia the delay in podset may be in excess of 1 month in existing chickpea growing areas (Berger et al., 2004), and more than 2 months if the crop is grown in cool southern areas such as Mt. Barker in West Australia (34.6 8S, 117.6 8E). Similar problems are encountered in northern Indian production areas in Haryana (Berger et al., 2006), Uttar Pradesh, and the Punjab (pers. comm. J.S. Sandhu). The situation is exacerbated in early flowering material because the probability of encountering low temperatures during the reproductive phase is increased (Berger et al., 2004). This sets up a dilemma for breeders: early phenology is essential for drought escape, and a requirement for wide adaptation, but increases the risk of establishing wasteful cycles of flowering and abortion. Clearly, there is a need for increasing reproductive chilling tolerance in chickpea to optimize the capacity for drought

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escape through early phenology. Considerable research has been directed at identifying the causal mechanisms underlying reproductive chilling sensitivity (Savithri et al., 1980; Srinivasan et al., 1998, 1999; Croser et al., 2003; Clarke and Siddique, 2004; Nayyar et al., 2005a,b). However, to date there has been no systematic search for reproductive chilling tolerance, and accordingly there is little diversity for this trait in chickpea. Much of the most tolerant material is derived from crosses involving a common parent originating from the former USSR (Croser et al., 2003), but this material has limited tolerance at temperatures <12–14 8C (Berger et al., 2005). As a result, increasing reproductive chilling tolerance remains an important breeding priority in Australia (Knights and Siddique, 2002) and India (pers. comm. J.S. Sandhu, P.M. Gaur). There are >68,500 chickpea accessions in the world’s genebanks (WIEWS, 2006), and screening all for reproductive chilling tolerance is simply infeasible. This paper describes two approaches to the systematic search for reproductive chilling tolerance which can be exploited for chickpea improvement. The first is an ecogeographic approach based on an agroclimatic analysis of global chickpea habitats in both time and space using high resolution interpolated climate models (Hijmans et al., 2001, 2005; New et al., 2002) to identify cool regions which are likely to select for reproductive chilling tolerance in locally adapted germplasm. Important questions include: where are the areas which stay consistently cool over the reproductive phase, and how common are they? Are these regions well sampled in world germplasm collections? What are the evolutionary implications of the distribution of reproductive phase temperatures among chickpea habitats? The second approach is based on the evolutionary divergence of chickpea from its annual wild relatives. In contrast to the cultigen, these are Mediterranean winter annuals subject to moderate to low winter temperatures (Berger et al., 2003) which appear to select for more low temperature tolerance than is found in chickpea (Singh et al., 1998; Abbo et al., 2002; Berger et al., 2005). This paper reviews the evidence for low temperature tolerance in the annual wild Cicer species, and highlights the current limitations to exploiting this resource in the improvement of cultivated chickpea. 2. Materials and methods Global chickpea growing regions were defined in Berger and Turner (2007) by mapping all accessions with latitude/ longitude data from the world’s principal collections, and modified using pre-existing maps (Cubero, 1980; van der Maesen, 1984; Saxena et al., 1996). For areas without extensive germplasm collections or pre-existing maps, such as North America and Australia, production regions were defined with feedback from local chickpea breeders. Distribution shapefiles were converted into 10’ grids (ca. 16 km resolution) using DIVA-GIS (Hijmans et al., 2001) and climate data extracted (Hijmans et al., 2005) for each grid-point. In order to identify areas where chickpea is likely to experience reproductive chilling stress it is necessary to define growing seasons in time throughout the crop’s global

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Table 1 Germplasm frequency from consistently cool flowering phase habitats in ICARDA, ICRISAT, USDA and ATFCC collections Habitat category

Cool flowering phase (<15.5 8C, Z-1)

Very cool flowering phase (<12.5 8C, Z-2)

Low seasonal temperature change (0.0 < 0.67 8C/day)

Chile (n = 4)

80

Intermediate seasonal temperature change (0. 67 < 0.135 8C/day)

Iberian peninsula (n = 11), Bulgaria (n = 2), North Africa (n = 1), Afghanistan (n = 3), South Asia (n = 1), Ethiopia (n = 46), Chile (n = 12) Iberian peninsula (n = 52), North Africa (n = 22), South Asia (n = 4)

Iran (n = 1), South Asia (n = 13)

92

Total

154

18

production regions. Chickpea growing seasons were regionally defined into typical months of sowing, flowering and maturity using published data and feedback from local breeders (Table 1). Within the WANA region the traditional spring sowing date for chickpea is negatively correlated to winter temperature (Berger and Turner, 2007), and determines the growing season climate. Climate data from field trials comparing autumn and spring-sown chickpeas in Lebanon, Syria, Turkey and Greece indicate mean monthly spring sowing temperatures of 10 8C (Singh et al., 1997; Iliadis, 2001; Ozdemir and Karadavut, 2003). Accordingly, a 10 8C monthly average sowing rule was adopted for chickpeas in WANA and the Mediterranean basin, with flowering occurring 3 months later. In the Indian subcontinent sowing varies from early October in the south to early November in the north, and both flowering and maturity are positively correlated with latitude (Berger et al., 2006). These relationships, based on 17 site means from 17.35 8N to 29.01 8N, were used to model South Asian chickpea growing seasons regionally: (a) flowering days after sowing = 3.12latitude 3.68, r2 = 0.73; (b) maturity DAS = 4.23latitude + 23.64, r2 = 0.82. The results were confirmed by breeders in Nepal, southern, central and northern India. Because these regressions calculate individual days of flowering and maturity for each grid unit, it was necessary to convert these data into months to comply with the monthly output of interpolated climate models. Based on the assumption that monthly temperature averages are likely to apply best in the middle period, while the beginnings and ends will reflect preand proceeding months, months were divided into thirds and the following rule applied: (a) 1st third, average temperature is based on mean of current and preceding month; (b) 2nd third, average temperature is based on mean of current month; (c) 3rd third, average temperature is based on mean of current and proceeding month. Note that this methodology effectively builds some slack into the regression output, making it more representative of typical farmer practice, where there will be changes in sowing date and subsequent phenology as a result of seasonal variation. To define reproductive chilling stress, long term average temperatures for the flowering period modeled for each grid point in the chickpea distribution shape file were extracted. The peak rate of temperature change within the growing season was modeled by regressing monthly temperatures from the coldest season month until maturity against day of year for each grid point. Average flowering phase temperatures and the peak

Total

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seasonal slopes of temperature increase were plotted as ordinal categories on the chickpea distribution map using DIVA-GIS (Hijmans et al., 2001). 3. Results Flowering phase temperatures <14 8C are uncommon across the chickpea distribution range (Fig. 1). Mediterranean climates in the southern hemisphere such as southern Australia and Chile tend to be uniformly cool during flowering, as do California and Portugal in the north (Fig. 2). Throughout most of the WANA region spring-sown chickpea experiences moderate to warm temperatures during flowering, with exceptions in coastal north Africa, the Nile valley and higher elevations in Morocco, the Balkans, and southwestern Iran. Ethiopia contains a wide range of flowering phase temperatures from the very hot near the Sudanese and Eritrean borders, to relatively cool in the uplands in the centre of the country. In the Indian subcontinent flowering phase temperatures tend to decrease with increasing latitude, with the warmest regions in Tamil Nadu and Andhra Pradesh, and the coolest adjoining the Himalayan foothills from the Nepali terai in the east, to the northern Pakistani Punjab in the west (Fig. 2). Mapping the peak rate of temperature change within the growing season makes it possible to assess which regions are

Fig. 1. Frequency histogram for mean flowering phase temperatures across the global chickpea distribution range.

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Fig. 2. Mean temperature of flowering phase throughout the global distribution of chickpea. Temperature categories were defined by Z scores in order to relate to the normal distribution presented in Fig. 1. Note that it was not possible to define chickpea phenology across the entire global distribution (see Table 2), therefore there are missing values in East Africa, Central Europe and Central Asia.

likely to experience relatively stable temperatures during the reproductive phase (Fig. 3). In South Asia the latitudinal temperature trend seen in Fig. 2 is reversed: the cool northern areas warm up much more quickly within the growing season, than do those in the south. Similarly, there is little growing season temperature fluctuation in the low latitude chickpea habitats of Ethiopia. However, the rate of increase in the landlocked Eastern Mediterranean Basin is high, moderating only near the maritime boundaries, and in Western Turkey and much of the Balkan region. There is intermediate seasonal temperature change in much of the Western Mediterranean, less near the western maritime regions, and more inland. Similarly, most of Australia has an intermediate growing season temperature change, except for the maritime areas in the south and west. There is relatively little temperature fluctuation in the American chickpea growing habitats; only California and southern Mexico are intermediate. Superimposing flowering temperatures on areas of low and intermediate seasonal temperature change identifies consistently cool regions where there is likely to be considerable selection pressure for reproductive chilling tolerance (Fig. 4). Across its global production range, chickpea is very rarely exposed to

temperatures <12.5 8C in environments where there is relatively low seasonal temperature change (>0.0 < 0.67 8C/day). Moderately cool temperatures (>12.5 < 15.5 8C) with low seasonal fluctuation are also uncommon, being confined to western Portugal, southern Australia and Chile, and isolated patches in the Ethiopian highlands, central Afghanistan, the Pacific Northwest USA, and Mexico. Very cool flowering phases in intermediate seasonal temperature change habitats (<12.5 8C and >0. 67 < 0.135 8C/day, respectively) are similarly rare, occurring in SE Australia, N South Asia, and SW Iran. The most widespread category are regions with moderately cool temperatures and intermediate seasonal fluctuation, occurring across the bulk of the Australian, Californian and Portuguese production areas, and smaller zones in N South Asia, SW Iran, the Nile Valley, maritime North Africa and Spain. 4. Discussion 4.1. Evolution The principal finding in this ecogeographic analysis of global chickpea production habitats is that the crop is rarely

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Table 2 Chickpea growing season and phenology across the world’s principal production areas Country

Climate

Sowing

Flowering

Maturity

Reference

Australasia Australasia Australasia East Africa East Africa Mediterranean Basin (West) Mediterranean Basin (West)

Australia (S) Australia (NE) Australia (NW) Ethiopia Sudan Greece Italy

Mediterranean-type Summer-dominant rainfall Summer-dominant rainfall Summer-dominant rainfall Summer-dominant rainfall Mediterranean-type Mediterranean-type

May–June May–June April–May September September–November March–April February–April

September August June–July November November–January May June

October–November September–October September January–February January–March June–July June–July

Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean

Basin Basin Basin Basin Basin Basin Basin

(West) (West) (WANA) (WANA) (WANA) (WANA) (WANA)

Portugal Spain Algeria Egypt Iran Iraq Israel

Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type

April–June January–February April–July March–June March–May

June–July April June–August June–July June–July

Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean Mediterranean

Basin Basin Basin Basin Basin Basin

(WANA) (WANA) (WANA) (WANA) (WANA) (WANA)

Jordan Lebanon Morocco Syria Tunisia Turkey

Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type Mediterranean-type

February–March March February–April November December, February–May February–April December–February, March–April March March February–April February–April February–March February–May

(Berger et al., 2004) Pers. comm. C. Douglas Pers. comm. T. Khan (Bejiga and Eshete, 1996) (Faki et al., 1996) (Iliadis, 2001) (Janneli and Bozzini, 1987; Saccardo and Calcagno, 1990) (Barradas, 1990) (Cubero et al., 1990; Rubio et al., 2004) (Maatougui et al., 1996) (Khattab and El-Sherbeeny, 1996) (Sadri and Banai, 1996; Soltani et al., 2001) (Abbas et al., 1996) Pers. comm. S. Abbo

April May April–June April–May April–May April–July

June June June–July June June–July June–Aug

Central Asia South Asia South Asia

Afghanistan Bangladesh India, Northern

Mediterranean-type March–April Summer-dominant rainfall October–November Summer-dominant rainfall October–November

January–February

March–April March–April

South Asia

India, Southern

Summer-dominant rainfall October

November–December January–February

South Asia North America North America

Nepal Canada Mexico, (W: Jalisco, Michoaca´n, Guanajuato) Mexico, (NW: Sinaloa, Sonora, Baja California Sur) USA, California USA, Northern Plains USA, Pacific Northwest Chile

Summer-dominant rainfall October–November Summer-dominant rainfall May Summer-dominant rainfall October

February–March July December

April September March

(Masadeh et al., 1996) (Singh et al., 1997) (Amine et al., 1996) (El-Ahmed et al., 1996; Singh et al., 1997) (Haddad et al., 1996) (Kusmenoglu and Meyveci, 1996; Ozdemir and Karadavut, 2003) (van der Maesen, 1972) (Abu Bakr et al., 2002) (Berger et al., 2006); pers. comm. J.S. Sandhu, S.S. Yadav, S.J. Singh, S.K. Chaturvedi (Berger et al., 2006); pers. comm. P.M. Gaur, H.S. Yadava Pers. comm. R. Shrestha Pers. comm. T. Warkentin Pers. comm. Pedro Manjarrez

Summer-dominant rainfall October–December

November–February

March–May

Pers. comm. Pedro Manjarrez

Mediterranean-type Summer-dominant rainfall Mediterranean-type Mediterranean-type

March–April June June November

June–July July–September August–September February–March

Pers. comm. F. Muehlbauer (Nielsen, 2001); pers. comm. F. Muehlbauer Pers. comm. F. Muehlbauer Pers. comm. M. Mera

North America North North North South

America America America America

November–December April–May April–May August–September

Note that in the Mediterranean Basin the traditional spring-sowing season is listed because this is the system under which locally adapted landraces evolved. Since there was no published data or local breeder feedback on chickpea phenology and distribution in East Africa, Central Europe and Central Asia, it was not possible to define growing season across the entire global distribution of the crop.

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Region

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Fig. 3. Peak rate of growing season temperature change throughout the global distribution of chickpea. Note that it was not possible to define chickpea phenology across the entire global distribution (see Table 2), therefore there are missing values in East Africa, Central Europe and Central Asia.

exposed to consistent reproductive chilling stress across its habitat range, except in new areas such as Australia, where the issue has been recognized as a breeding priority (Knights and Siddique, 2002; Berger et al., 2004; Clarke et al., 2004). This reflects the crop’s distinct evolutionary path which separates it from the remainder of the West Asian Early Neolithic founder crop assemblage (Abbo et al., 2003a,b). Whereas crops such as wheat, barley and pea remained as winter annuals after domestication and were disseminated across a wide longitudinal and latitudinal range, chickpea-domesticated from the Mediterranean winter annual Cicer reticulatum Ladz. (Ladizinsky and Adler, 1976), changed into a spring-sown crop early in its evolution, with profound effects on its subsequent habitat range (Abbo et al., 2003a). The distribution of chickpea archeological remains is biphasic in time, with 14 Neolithic sites older than 5500BC, and 18 Bronze Age finds from 2800 to 1300 BC (Redden and Berger, 2007), but only a single intervening appearance in Dimini, Greece, in 3500 BC (Kroll, 1979). It has been suggested that the disappearance of chickpea from West Asia in the Late Neolithic was as a result of Ascochyta disease pressure on the winter crop, and that its subsequent reappearance, which coincided with the development of summer cropping, was as a spring-sown crop which could avoid the peak winter disease

period (Abbo et al., 2003a,b). This is confirmed by the earliest written records and traditional farming practices which establish chickpea as a long-standing spring-sown crop in the Mediterranean Basin (Theophrastus, 1916; Pliny, 1938; Abbo et al., 2003b). If it is accepted that chickpea was grown as spring-sown, post-rainy season crop in WANA from the early Bronze Age onwards, then it is likely that this change in farming system preselected chickpea for subsequent dissemination to warm semiarid climates to the south and east. The chronology and location of archeological finds support in this hypothesis. From 2000 to 1000 BC, chickpea remains become increasingly common in south and east of the West Asian domestication heartland, occurring in present-day Iraq (n = 1), Pakistan (n = 2), India (n = 11), and Egypt (n = 1) (Redden and Berger, 2007). Finally, by 290 BC chickpea appeared in Ethiopia (Dombrowski, 1970). The West Asian shift from winter-annual to spring-sown crop in and subsequent dissemination to the south and east reduced chickpea’s exposure to cold stress. Chickpea production regions in WANA experience cold winters (mean = 4.3 8C, (Berger and Turner, 2007)), and since spring-sowing also delays the onset of flowering by up to 1 month (Singh et al., 1997; Iliadis, 2001; Ozdemir and Karadavut, 2003), springsown crops in WANA tend to escape low temperature stress

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Fig. 4. Consistently cool flowering habitats in the world’s key chickpea production areas defined by superimposing cool to very cool extremes of the chickpea flowering temperature distribution (<15.5 8C, Z-1; <12.5 8C, Z-2) on regions with low and intermediate seasonal temperature change.

throughout their lifecycle-including the reproductive phase. Moreover, the present analysis suggests that in spreading south and east, chickpea predominantly established niches in habitats with similar, or warmer flowering phase temperatures, except in northern South Asia, where the chilling stress is likely to be transient, given the rapid increase in temperature throughout the growing season in this region. Fig. 4 shows that consistently cool flowering phase habitats are particularly rare in the WANA and South Asian regions where chickpea evolved as a crop, and suggest that reproductive chilling tolerance is likely to be uncommon. This is confirmed by field evaluations which measured both flowering and podding in genotypes from diverse origins, but did not find new sources of chilling tolerance (Berger et al., 2004, 2005). Unlike the cultigen, the wild relatives of chickpea grow as winter annuals from West to Central Asia, and appear to be exposed to considerably greater cold stress throughout their lifecycle (Berger et al., 2003). Accordingly, their response to cold stress differs markedly from cultivated chickpea. Whereas chickpea is unresponsive to vernalizing temperatures (30 days at 4 8C), annual wild Cicer species other than C. yamashitae

respond by advancing the dates of flowering, podding and maturity (Abbo et al., 2002; Berger et al., 2005). Cold winters (temperatures from 2.3 to 4.0 8C) tend to damage chickpea seedlings significantly more than most annual wild Cicer species, causing leaflets and branches to wither (Singh et al., 1990). In an early evaluation of vegetative cold tolerance, only 15 of 5515 chickpea accessions were tolerant (Singh et al., 1990). Similarly, when reproductive chilling tolerance was evaluated at a cool field site (13.1 8C) the annual wild Cicer species were significantly less sensitive than the cultigen (Berger et al., 2005). However in this study, which evaluated a large proportion of the world’s collection of original accessions, the combination of early flowering and chilling tolerance was only found in C. pinnatifidum and C. judaicum, neither of which are in the primary gene pool of chickpea. 4.2. Strategies for finding reproductive chilling tolerance in cultivated chickpea The preceding discussion points to two different strategies to optimize the search for reproductive chilling tolerance. In

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cultivated chickpea, evaluating germplasm from consistently cool flowering phase habitats is a priority. Landraces are preferred, because these will have a long history of exposure to chilling temperatures at flowering, and it is assumed that this stress will have selected for an adaptive response in the germplasm. Adaptation to reproductive chilling stress may involve a wide range of mechanisms. In the relatively chilling tolerant genotypes developed from the former Soviet accession K 1189 (ICC 8923) tolerance was conferred by the capacity to fertilize a higher percentage of ovules, associated with greater ovule viability, and higher in vivo pollen germination and subsequent tube growth (Srinivasan et al., 1999; Clarke and Siddique, 2004). However, since exposure of chickpea to chilling temperatures also increases oxidative stress, electrolyte leakage, polyamine concentrations, and decreases respiration, relative water content, chlorophyll content, carbohydrate concentrations in aborted flowers, seed filling, root growth and yield (Nayyar and Chander, 2004; Nayyar et al., 2005a,b), there is potential for a wide range of resistance mechanisms in the crop. The fact that plants, including cultivated annuals, can ameliorate many of these chilling-induced injuries by acclimation (Croser et al., 2003; Bakht et al., 2006) strengthens the suggestion that consistently cool habitats are likely to be particularly important in the search for reproductive chilling tolerance in chickpea. Unfortunately, the world chickpea collection contains relatively little germplasm from consistently cool flowering phase habitats (Table 1). This shortcoming is exacerbated by the lack of passport data in potentially interesting regions. For example, the USDA collection contains 1315 accessions from Iran, but only 2 with latitude/longitude data, and 7 with locality names (USDA-ARS, 2006). On this basis it is impossible to ascertain the likelihood of germplasm coming from cool flowering habitats in Fars province, for example. Similarly, the lack of data from Central Asia is problematic, given the only known source of cultivated chilling tolerance comes from the former USSR (Croser et al., 2003). To address this problem, existing germplasm collections should be augmented by maximizing data retrieval from the original collection records wherever possible. For example, using gazetteers and GIS software it is possible to generate approximate collection site coordinates from locality names, and subsequently characterize site climate using the techniques detailed in the present study. Then it becomes feasible to design experiments to evaluate germplasm from contrasting temperature environments which should expedite the discovery of reproductive chilling tolerance, and will contribute significantly to our understanding of chickpea adaptation. In chickpea the concept of crop ecology is in its infancy (Berger and Turner, 2007). There is little published information on how and why germplasm from different habitats differs in response to differential environmental selection pressures. Chickpea appears to operate as a typical competitive ruderal, where reproductive strategies become increasingly conservative as habitats become more stressful or uncertain (Grime, 1979). Thus, South Asian germplasm from short season

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habitats in Gujarat, southern and central India is characterized by early phenology, low yield responsiveness, low biomass, and high harvest index (Berger et al., 2006). Conversely, genotypes from northern India had later, highly responsive phenology, and could delay flowering significantly more at late flowering, northern sites. Extending the vegetative phase under long season conditions increased biomass accumulation prior to reproduction in this well-adapted material, and delayed flowering until temperatures became sufficiently warm to support pod set (Berger et al., 2006). Whether delayed phenology is a consistent response to cool climates in the chickpea production range is a compelling issue to address in the search for reproductive chilling tolerance. It is tempting to speculate that delayed phenology may be selected for in transiently cool environments such as much of northern South Asia, but perhaps not in the more consistently cool habitats listed in Table 1. 4.3. Strategies for finding reproductive chilling tolerance in annual wild Cicer species The second strategy for improving reproductive chilling tolerance in chickpea is to concentrate on the annual wild Cicer species in order to exploit both their higher tolerance to cold stress and increased genetic diversity relative to the cultigen. The principal limitation to this approach is the lack of germplasm in the world collection. In contrast to chickpea, the world’s annual wild Cicer collection is both well characterized in terms of passport data and small (Berger et al., 2003). Apart from C. judaicum which has recently been augmented by substantial new collection in Israel (Ben-David et al., 2006), there are <30 original accessions in each of the 8 annual wild Cicer species. In the primary gene pool of chickpea, the collection is particularly weak: there are 10 independent accessions of C. echinospermum P.H. Davis, and 18 of C. reticulatum Ladzinsky (Berger et al., 2003). These low numbers dictate that no single annual wild Cicer species has been meaningfully characterized, because the adaptive potential of a species cannot be adequately described with such low sample sizes. More collection and field observation of phenology is urgently required, particularly from eastern Anatolia to north western Iran, and northwards into the Caucasus. Based on existing genetic resources a thorough evaluation of reproductive chilling tolerance in accessions subsampled from the original collections is warranted. Previous work (Berger et al., 2005) has concentrated exclusively on material originally collected from the wild, and may have missed useful material. Future field screening should use early and standard sowing dates so that late flowering material can be evaluated under chilling temperatures. In the earlier evaluation of wild Cicer reproductive chilling tolerance (Berger et al., 2005), genotypes flowering in mid spring (October onwards; ca 41% of accessions) experienced warmer post-anthesis temperatures than those flowering in September (13.7 and 11.6 8C, respectively). Consequently, late flowering, chilling-tolerant material may not have been identified.

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5. Conclusions This study has demonstrated that chickpea is rarely found in habitats which experience chilling temperatures during the reproductive phase, probably as a consequence of its unique evolution and subsequent dissemination. Nevertheless, there are significant differences in the capacity of chickpea and its wild relatives to set pods under low temperature stress, indicating that the search for reproductive chilling tolerance is worthwhile. However, our capacity to conduct such a systematic search is constrained by: (a) the low proportion of chickpea germplasm which can be climatically characterized because of the lack of information on origin (latitude/longitude or locality name) listed on genebank databases; and (b) the extremely low number of annual wild Cicer accessions in the world collection, which preclude a meaningful assessment of species’ potential. While both issues are important for improving chilling tolerance in chickpea, they have broader ramifications in facilitating a comparative physiological approach to adaptation research where wild and cultivated germplasm can be compared across a wide range of habitats, and should therefore be supported. Acknowledgements The author would like to acknowledge generous research funding support from the Department of Education, Science and Training (DEST), Commonwealth Scientific and Industrial Research Organisation (CSIRO), the Centre for Legumes in Mediterranean Agriculture at the University of Western Australia (CLIMA), the Australian Centre for International Agricultural Research (ACIAR) and the Australian Grains Research and Development Corporation (GRDC). Mapping the global chickpea distribution and modelling growing seasons would not have been possible without generous feedback and advice from the global community of breeders and scientists, including: Fred Muehlbauer, Mario Mera, Tom Warkentin, Renuka Shrestha, Shahal Abbo, Pedro Manjarrez, Kadambot Siddique, Robert Hijmans, Dirk Enneking, Col Douglas, Kharaiti Mehra, Jason Brand, William Martin, Michael Materne, Larn McMurray, Eric Armstrong, Tanveer Khan, J.S. Sandhu, Harsh Nayyar, Jan Konopka and Ted Knights. References Abbas, A.I., Ali, A.H., Ibrahim, K.S., 1996. Chickpea in Iraq. In: Saxena, N.P., Saxena, M.C., Johansen, C., Virmani, S.M., Harris, H. (Eds.), Adaptation of Chickpea in the West Asia and North African Region. ICRISAT, ICARDA, Hyderabad, India; Aleppo, Syria, pp. 35–46. Abbo, S., Berger, J.D., Turner, N.C., 2003a. Evolution of cultivated chickpea: four genetic bottlenecks limit diversity and constrain crop adaptation. Funct. Plant Biol. 30, 1081–1087. Abbo, S., Lev-Yadun, S., Galwey, N., 2002. Vernalization response of wild chickpea. New Phytol. 154, 695–701. Abbo, S., Shtienberg, D., Lichtenzveig, J., Lev-Yadun, S., Gopher, A., 2003b. The chickpea, summer cropping, and a new model for pulse domestication in the ancient near east. Q. Rev. Biol. 78, 435–438. Abu Bakr, M., Ali Hussein, S., Ali Afzal, M., Rahman, M.A., 2002. Chickpea status and production constraints in Bangladesh. In: Bakr, M.A., Siddique,

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