Plant Science 215–216 (2014) 48–58

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Review

Could abiotic stress tolerance in wild relatives of rice be used to improve Oryza sativa? Brian J. Atwell ∗ , Han Wang, Andrew P. Scafaro Department of Biological Sciences, Faculty of Science, Macquarie University, New South Wales 2109, Australia

a r t i c l e

i n f o

Article history: Received 21 July 2013 Received in revised form 28 September 2013 Accepted 11 October 2013 Available online 21 October 2013 Keywords: Biogeography Breeding Climatic distribution Introgression Oryza Wild relatives

a b s t r a c t Oryza sativa and Oryza glaberrima have been selected to acquire and partition resources efficiently as part of the process of domestication. However, genetic diversity in cultivated rice is limited compared to wild Oryza species, in spite of 120,000 genotypes being held in gene banks. By contrast, there is untapped diversity in the more than 20 wild species of Oryza, some having been collected from just a few coastal locations (e.g. Oryza schlechteri), while others are widely distributed (e.g. Oryza nivara and Oryza rufipogon). The extent of DNA sequence diversity and phenotypic variation is still being established in wild Oryza, with genetic barriers suggesting a vast range of morphologies and function even within species, such as has been demonstrated for Oryza meridionalis. With increasing climate variability and attempts to make more marginal land arable, abiotic and biotic stresses will be managed over the coming decades by tapping into the genetic diversity of wild relatives of O. sativa. To help create a more targeted approach to sourcing wild rice germplasm for abiotic stress tolerance, we have created a climate distribution map by plotting the natural occurrence of all Oryza species against corresponding temperature and moisture data. We then discuss interspecific variation in phenotype and its significance for rice, followed by a discussion of ways to integrate germplasm from wild relatives into domesticated rice. Crown Copyright © 2013 Published by Elsevier Ireland Ltd. All rights reserved.

Contents 1. 2. 3.

4.

Introduction to the genus Oryza and evolution of modern cultivated rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Using climate distribution models to identify useful wild rice species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Exploiting phenotypic diversity of wild rice relatives for crop improvement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Vegetative morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Mesophyll characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Secondary metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Abiotic stress–response pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introgressing genes from wild rice relatives into O. sativa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Introgression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Weediness and escape. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction to the genus Oryza and evolution of modern cultivated rice Cultivated rice has evolved from its wild progenitors through a series of introgressive events, natural selection and ultimately,

∗ Corresponding author. Tel.: +61 2 98508224. E-mail address: [email protected] (B.J. Atwell).

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breeding. By these processes, just two of the 24 extant species have become agronomically productive, namely Oryza sativa from Asia and Oryza glaberrima from Africa. The other 22 wild species have native distributions spanning all tropical and subtropical regions of the world, throughout much of Africa, South-East Asia, Australasia and Central and South America [1,2]. There is evidence of human consumption of wild rice species from China dating back 13,000 to 14,000 years [3] and O. sativa was present in that region 6600 years ago. The common

0168-9452/$ – see front matter. Crown Copyright © 2013 Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.plantsci.2013.10.007

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cultivated species of rice from Asia, O. sativa, seems to have arisen through domestication of the wild species Oryza rufipogon and Oryza nivara [4–8]. Events leading to domestication are described in recent major reviews [9,10]. In brief, one theory proposes a ‘snowballing’ model, wherein a core of domestication genes spread to neighbouring populations. Critical among these genes was sh4 mutation which is responsible for reduced shattering thus enabling grain to be harvested [11]. Alternatively, the combination model proposes separate domestication events from divergent wild rice populations, leading to disparate domesticated rice genotypes. There are two distinct sub-species of O. sativa – japonica and indica – alongside several less common sub-populations [4]. While it has been suggested that the two sub-species diverged 100,000 years ago [4], the chronology of domestication remains speculative. Detailed genomic studies have since been performed on diverse populations of O. rufipogon, assuming that this species is the ancestral progenitor of modern rice [12]. The evidence indicates that the first japonica rice arose from a specific O. rufipogon population in southern China. Sub-species indica is purported to be the result of introgressions from wild relatives that occurred as this japonica sub-species spread into South-East and South Asia [12]. A second cultivated rice species, O. glaberrima, appeared 2000–3000 years ago through a separate domestication process in which the native African grass, Oryza barthii, was artificially selected for human use [13]. Since domestication, introgression of wild germplasm from cross-compatible species such as O. rufipogon sharing the AA genome with O. sativa has been a natural and on-going process [14,15]. Introgression of genes from wild rice to O. sativa can occur due to the variable degrees of out-crossing and the close proximity between Oryza species, particularly in Asia [16]. There are approximately 120,000 cultivated rice accessions (including landraces) in existence today, with O. sativa dominant among commercial rice genotypes [17]. Despite there being so many accessions in germplasm banks [18] and a further half a million landraces purportedly in existence, O. sativa has still substantially less genetic diversity than its progenitors and congeners combined; most estimates claim the proportion to be less than half the diversity found in wild relatives of Oryza [7,19,20]. Some wild relatives have genomes three times the size of O. sativa [21,22], arising through major transpositions in the genome. O. glaberrima, the domesticated species of rice from Africa, has even less genetic diversity than its Asian counterpart [13]. Clearly, only a small percentage of the progenitor population was sourced during the domestication process [19,20,23]. It is likely that all crop species have undergone a genetic bottleneck and subsequent loss of genetic diversity during the early stages of domestication [24], but the extent of the genetic loss is species-specific. For example, soybean (Glycine max) has close to 50% of the genetic diversity found in its wild progenitor, Glycine soja [25,26]. Maize (Zea mays ssp. mays) seems to have maintained a higher level of genetic diversity despite a domestication bottleneck, containing upwards of 60% of the genetic diversity found in Zea mays ssp. parviglumis, the wild progenitor [27]. Maize has probably maintained higher genetic diversity during domestication through outcrossing while rice, which is to varying degrees self-pollinating, appears to have had less introgression of DNA from wild relatives [23]. This effect could have been accentuated by the diminished opportunity for out-crossing in intensive rice cultivation systems, which are generally separated from wild Oryza populations. The phenotypic contrast between modern and wild relatives of rice (e.g. O. rufipogon) would suggest that domestication arose with selection for only a few key traits, including non-shattering, absence of secondary dormancy, fewer and more upright tillers and lack of colouration [4,6,11,12,28,29]. An annual habit was probably selected early in cultivation. Both vegetative characteristics

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and seed properties have contributed to the success of rice as a food source for humanity, along with inadvertent selection of more subtle features such as increased mesophyll conductance [30] and a complex of genes involved in cooking properties [31]. However, it is now becoming apparent that future cultivation of domesticated species must extend beyond the ever-shrinking supply of arable land and accommodate a more variable global climatic regime [32]. Selecting for traits allowing for the mitigation of abiotic stresses has now moved to the forefront of crop improvement. Much of the focus on improving rice cultivars is still centred on sourcing the genetic diversity found in O. sativa [33]. However, the use of germplasm from wild relatives to improve domesticated rice is destined to be an increasingly urgent priority [10,24,34] as demonstrated for biotic stress traits [35,36]. Initial approaches are likely to concentrate on close relatives of rice as these species harbour many desirable traits that are reasonably accessible via conventional breeding. However, transgenes from taxonomically remote species will eventually be exploited in rice genetics. Recent progress in sequencing the genomes of many species in the Oryza genus is one more step in identifying the genetic differences often associated with yield and abiotic factors such as heat, chilling, flood tolerance and drought [37]. Those features that result from posttranslational and epigenetic effects, such as the floral switch, will be less easily manipulated in cultivated rice. The introgression of genes that encode abiotic stress tolerance could be detrimental if they are linked negatively to yield, necessitating detailed physiological analysis of novel hybrid Oryza lines. For example, selection for upland rice might demand more extensive root systems at a cost to aboveground biomass accumulation. Considering the pan-tropical natural distribution of wild rice species across biomes ranging from equatorial to savannah, and the demonstrated genetic diversity that accompanies this spectrum of environments, these wild species are an untapped resource for improvement of cultivated rice and other cereals (Fig. 1). Geographically separated and highly localised habitats in which wild rice species are found have led to strong intraspecific genetic barriers, underlining the importance of conservation of small populations that might contain critical genes [1,38–40]. However, the costs of acquisition and conservation have meant that there is a still a modest bank of only 4500 wild Oryza relatives held at the International Rice Research Institute (Jena, pers. comm.). In this review, we explore three aspects of incorporation of germplasm from wild rice relatives into cultivated rice. Firstly, we present climate–distribution relationships based on some climatic factors that we propose have driven the natural distribution of wild rice species. This modelling is presented to identify sources of Oryza germplasm suitable for individual stress tolerance mechanisms. As a development of this approach, we have applied future climate simulations to these climate–distribution relationships, using China and India as case studies. Secondly, we highlight individual examples of phenotypic variation in metabolism and development, indicating potential targets for genetic gain in cultivated rice. Thirdly, we briefly describe methodologies and their limitations for introgression of genes from wild rice species into cultivated rice.

2. Using climate distribution models to identify useful wild rice species The 24 Oryza species have a pan-tropical distribution (Fig. 1), with most species unique to a single continent but some with a broader distribution, such as O. rufipogon which extends from Asia into Australia, and Oryza eichingeri, which is common to Africa and Sri Lanka [1]. Uniquely, Oryza punctata exists in both diploid and tetraploid forms in Africa but occupies distinct niches, with the diploid form in more exposed landscapes [1]. In spite of some

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Fig. 1. Distribution of all the wild rice species according to collection sites described in Vaughan [2] and the Gateway to Genetic Resources (http://www.genesys-pgr.org/). Annual species are represented by triangles, perennial species by circles and O. punctata (which is either annual or perennial depending on ploidy) by a square. These distinctions are not categorical because the growth habit of several species are indeterminate or biennial.

wild Oryza species such as those from the Oryza ridleyi and Oryza granulata complexes occurring in shady conditions and on forest floors where radiation loads are likely to be attenuated, all Oryza species are restricted to climatic zones that are sub-tropical to tropical during the growing season, where the mean temperature during the coolest months of the growing are above 15 ◦ C. In an effort to determine whether there is substantial genetic variation in the climatic requirements of the wild relatives of O. sativa, we extracted all known collection points for the 24 species across four continents and converted them to GPS coordinates. These data were sourced from two origins, namely Vaughan [2] and the Gateway to Genetic Resources (http://www.genesys-pgr.org/). Climatological data (monthly means of temperature, precipitation and cloud cover) for these locations were then extracted from Climate Research Unit (CRU) CL1.0 at the resolution of 0.5 degree. With a simple process-based bioclimatic model (STACH [41]) a suite of bioclimate factors, principally, moisture, radiation and temperature characteristics, could be estimated from these climatologies and connected with each species, resulting in the distributions depicted across Asia, South America, Australasia and Africa in Fig. 2. The grey shading on each figure represents the full range of climate observations across each continent, reflecting a range from arid hot climates to regions which are cold, by virtue of high altitude or latitude. The climate variables that we pursued were chosen according to what we believed to be key drivers of the natural distribution of the genus Oryza. These are presented as paired figures, the first being moisture related and the second temperature related. Specifically, the ordinate was the same in all figures; after eliminating climate data for the three coolest months when we assumed no growth of rice was likely, we inserted the mean temperature of the coolest month (MTCO) from the remaining nine months at each location. Even if rice did not grow throughout this nine-month period, we assumed that the coolest month reflected the likelihood of cold spells during the critical reproductive stage. For the first of each pair of figures, the abscissa was the ‘moisture index’ (MI), defined as the ratio of mean annual precipitation to annual equilibrium evapotranspiration, only as a function of net radiation and

temperature. As evident from Fig. 2, values of MI ranged from close on zero up to four; as values approached four, the site was considered to have copious available moisture. The second pair defined the abscissa to be the ‘growing degree days exceeding 15 ◦ C’ (GDD15 ) to reflect the heat sum available for growth, also over the nine warmest months. These data show a number of interesting trends, with the means (±standard deviation) in Fig. 2 and the raw data showing the entire range in Supplementary Fig. 1. In that rice development in cooler growing zones is sometimes analysed using 10 ◦ C as a base temperature, we present data calculated using this lower base in Supplementary Fig. 2. Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.plantsci. 2013.10.007. Key findings are: • Mean monthly temperatures below 20 ◦ C generally constrain distribution across the entire Oryza genus. Only 5% of all wild relatives were collected from sites with an MTCO (of the nine warmest months) below 20 ◦ C; 4–8% were from South America and Asia with none from Australasia and Africa. • The moisture and temperature habitats of Australian species are restricted to seasonally dry and hot environments, with the New Guinean species, Oryza schlechteri unique in that it is found in hot wet sites. • African species are similarly restricted to the hot and relatively dry regions of the continent, with Oryza barthi and O. glaberrima appearing to be the species most tolerant to arid conditions). • Asian and South American rice are generally restricted to wetter locations, with the possible exception of Oryza rhizomatis which grows in the driest and hottest of the available sites and is endemic to Sri Lanka. Collections of all O. rhizomatis accessions have notably all been made from the drier regions of that island nation, none coming from the wet central south-west. Phenotypic traits are selected through environmental pressure, reflecting the distribution of each species across its endemic climate range. For example, a recent study of 17 Oryza species [42]

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Fig. 2. Application of a simple process-based bioclimatic model to the global distribution of 21 species of Oryza collected from four continents. The collection sites are from two sources: Vaughan [2] and the Gateway to Genetic Resources (http://www.genesys-pgr.org/). Once GPS coordinates were determined, they were overlaid onto the distribution of climate data for the whole continent (in grey), with each species depicted in a unique colour. The climate variables used were: mean temperature of the coolest month among the nine warmest months at each location (MTCO); growing degree days above 15 ◦ C for the nine warmest months (GDD15 ); the ratio of mean annual precipitation to annual equilibrium evapotranspiration (MI). Means of all collection points for each species and standard deviations for each variable are depicted.

showed Oryza meridionalis, Oryza australiensis, O. glaberrima and Oryza longistaminata to have leaf traits, notably leaf thickness, correlating with transpiration efficiency and drought tolerance. These species come from Australia and Africa, in seasonally dry and hot environments, supporting the use of climatic indicators we have presented as predictors of interspecific adaptive traits to temperature and moisture stress. These distributions are a work in progress in that finer calibration of the grids and better understanding of the climate factors will help separate the species distributions. However, on the strength of the data we present, one can see that all Oryza species are strongly constrained by temperature. While freely available moisture is also essential to Oryza species, Supplementary Fig. 1 shows that the range of moisture indices over which the 22 species have evolved are quite diverse. Moisture status at the precise site of collection cannot be resolved in current models and is much more locally variable than the thermal regime. However, with these limitations, we use moisture index to indicate the excess of rainfall over evaporation and thus the likelihood of substantial bodies of water occurring, where rice species might have evolved. Perennial habit is likely to be adaptive in allowing rice to inhabit the extremes of these ranges, possibly due to the purportedly greater genetic diversity in these species [43]. This is indicated for O. rufipogon in Asia and O. longistaminata in Africa, where the standard deviations are relatively large for the temperature range they can occupy. Further field data are required for O. australiensis, which is strongly perennial and

tolerant to high radiation and seasonally very dry regions of Australia but remains under-represented in the dataset in Supplementary Fig. 1. According to this biogeographic analysis, species which might be used to source abiotic stress tolerance genes are listed in Table 1. More comprehensive collection of these species with regard to the microclimates in which they evolved is therefore a matter of the highest priority for genetic progress in breeding programmes. The conservation of wild rice populations which are dangerously imperilled in many parts of the four continents on which rice has speciated is equally pressing [37]. The relationship of wild Oryza species to current continental climate profiles (Fig. 2) gives a picture of the environments that have been conducive to survival of these wild accessions. However, this does nothing to inform us about whether these accessions were collected from locations that typify those to be expected in rice-growing countries 50–75 years from now. To address this, we plotted the current and 2070–2099 climate spaces (Fig. 3 – grey and pink dots, respectively) for China and India, overlaid by the distribution of wild Oryza collections worldwide. The gaol was to see whether the climatic shifts that might be expected in these major rice food bowls might be tackled by using germplasm from similar regimes. To achieve these ‘climate–shift’ figures, future climate scenarios for the period 2070–2099 were derived from a set of seven global climate model outputs, with the pattern scaled to yield a 2 ◦ C global warming by mid-century

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Table 1 Candidates for tolerance to particular abiotic stresses based on bioclimatic analysis presented above. Species with distributions at the temperature and moisture extremes were considered as likely candidates for abiotic stress tolerance. Plasticity refers to species with distributions over a wide temperature and moisture range (Supplementary Fig. 1). Species are listed in ascending order based on increasing extent of tolerance. Heat tolerance A. Extremes O. barthii (AA) O. australiensis (EE) O. meridionalis (AA) O. glaberrima (AA) O. longistaminata (AA)

Cold tolerance

Drought tolerancea

Flooding

O. granulata (GG)

O. barthii (AA) O. australiensis (EE) O. glaberrima (AA) O. longistaminata (AA) O. punctata (BB,BBCC)

O. schlechteri (HHKK) O. latifolia (CCDD) O. grandiglumis (CCDD) O. ridleyi (HHJJ)

Temperature

Moisture

B. Plasticity O. longistaminata (AA) O. punctata (BB,BBCC) O. meyeriana (GG) O. granulata (GG)

O. ridleyi (HHJJ) O. latifolia (CCDD) O. officinalis (CC) O. granulata (GG)

a As moisture availability in many cases is specific to the microhabitat in which a species is found (e.g. flood plain versus open scrubland) it is difficult to relate moisture index precisely to the moisture availability for individual populations, which might occur in isolated wetlands. Despite this, we assume an association between moisture index and availability of free water exists on the grounds that wet locations are more likely to produce more swamps, marshes, waterholes, ox-bows and billabongs.

To (http://www.cru.uea.ac.uk/∼timo/climgen/data/questgsi/). compare the current climate spaces with future regimes, the three bioclimatic variables (MTCO, MI, and GDD15 ) were re-calculated from the average values of each climate model projection, based on monthly mean values of temperature, precipitation and fractional sunshine. The data show several interesting features. Thermal sum (GDD15 ) will increase for both countries, in the case of India to levels up to 5000 degree days. Moisture index will change less but significant drying will be seen, particularly in China. Meanwhile MTCO will rise to above 25 ◦ C for most of India. Under these circumstances, the pink zones that are likely to represent future conditions coincide more closely with the climate regimes in which wild Oryza populations have been collected. Thus one might tentatively conclude that India will be the greater beneficiary of gene combinations coding for abiotic stress tolerance that can be found uniquely in wild Oryza species.

3. Exploiting phenotypic diversity of wild rice relatives for crop improvement 3.1. Vegetative morphology Artificial selection has shifted the vegetative traits of O. sativa, making modern commercial rice varieties distinct from its wild relatives. These contrasts range over many levels of organisation, including canopy architecture, leaf and sheath morphology, leaf structure and physiology. However, the robust growth rates that are required during a brief monsoonal growing season in parts of Africa and Australia and heavy accumulation of shoot biomass, as well as nutritious seeds, suggest that some wild Oryza species have properties that could benefit domesticated rice. The phenotype of the progenitors of modern crops varies widely, with seed mass in cereals such as rice and wheat having increased markedly through improved management and genetics (e.g. [44] for wheat;

Fig. 3. Future climate scenarios for the period 2070–2099, derived from a set of seven global climate model outputs, with the pattern scaled to yield a 2 ◦ C global warming by mid-century (http://www.cru.uea.ac.uk/∼timo/climgen/data/questgsi/). Bioclimatic variables (MTCO, MI, and GDD15 ) were plotted as for Fig. 1 (grey dots) and re-calculated from the average values of each climate model projection (pink dots). Blue symbols indicate collection sites for all known wild Oryza species.

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[45] for rice) while other species such as maize had high potential yields even centuries before modern agriculture [46]. For cereals, larger seed mass and improved harvest index generally offer the greatest scope for yield gain and would therefore be the highest criteria if wild species of Oryza species were ever to be domesticated. Leaf dimensions of O. sativa cultivars affect plant water demand [47]. Cultivars with broader and larger individual leaf area had greater transpiration efficiency under drought conditions, diminishing the impact of drought in these cultivars compared with those having slender foliage. Our own observations comparing the Australian species O. australiensis and O. meridionalis with a local commercial cultivar of O. sativa ssp. japonica revealed a spectrum of leaf dimensions, leading one to suggest tentatively that this phenomenon might hold across species. For example, the area of individual leaves of mature plants of the relatively drought-tolerant species, O. australiensis, was 50% larger than those of O. meridionalis and O. sativa, even though there were half as many leaves on O. australiensis at the early vegetative stage [48]. Large leaves with high investment in structural and vascular tissue might be a characteristic of rice species that are tolerant to periodically dry, hot savannah, in accordance with the general observation that plants from dry, hot environments have greater leaf mass per leaf area [49]. Similar measurements for Oryza species from Africa, particularly from the drier regions of that continent (Section 2), might reveal suitable donor phenotypes for genes encoding leaf dimensions and thereby, drought tolerance. A critical feature of plant domestication is the re-alignment of assimilate partitioning to maximise harvest index. Much progress has been made in the area of phloem transport and control of sink strength but the interaction of environmental factors – such as drought and nutrient imbalance – with patterns of photoassimilate allocation remains challenging [50]. O. rufipogon has much greater phenotypic plasticity in the allocation of biomass below ground and in shoot architecture than its close relative, O. sativa [51]. Furthermore this report showed that O. rufipogon had a greater plasticity in leaf sheath length than cultivated rice under three planting densities, independent of mean sheath length. A truly comprehensive quantification of morphological and developmental plasticity, particularly among those wild ecotypes from extreme environments identified in Section 2, could provide germplasm better adapted to the oscillations projected under future climate regimes. The extent of tillering might be especially important, with relatively unrestricted tillering optimal under abundant supply of water and nutrients. By contrast, under water deficits and short growing seasons, activation of tillers from dormant nodal buds should be genetically restrained to accommodate the limited resource supply. Vastly improved knowledge about the genetic control of axillary bud dormancy [52] will open the possibility of optimising tillering for diverse environments. However, tillering is only one aspect of canopy architecture, with tiller angle and leaf orientation attracting increasing attention in recent years. Crop canopy architecture is a developmental feature which varies significantly among species of rice, with a distinctly compact canopy in modern varieties of O. sativa at one end of the spectrum but wild relatives having variously open canopies (e.g. O. australiensis) or scrambling habits (e.g. Oryza minuta and O. rufipogon) [2]. We have used digitised three-dimensional imaging to observe that the efficiency of overhead solar radiation by the tall open canopy of O. australiensis was surprisingly similar to that of the co-occurring species, O. meridionalis, which had a denser canopy with dozens of tillers. However, light interception efficiency depends upon the angle of the incoming radiation, suggesting that canopy architecture could be genetically adapted for latitudes from equatorial to 40◦ N/S according to the distinctive radiation and heat load of sub-tropical and temperate zones. Seminal studies show

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that the trait locus, Ideal Plant Architecture 1, has dramatic effects on canopy erectness [53], which gives hope for canopy re-design appropriate to future climate regimes. 3.2. Mesophyll characteristics Subtle leaf features have become fixed in cultivated rice probably through indirect selection for improved yield. For example, at the cellular level, improved leaf mesophyll conductance has apparently become established in O. sativa compared with O. meridionalis and O. australiensis, the dominant wild Oryza Australian species [30]. Indeed, substantial variation in leaf cellular characteristics has been found across much of the genus Oryza [42]. However, it remains to be established whether such changes in subcellular structures have occurred passively through the process of domestication without a more thorough examination of species sharing the AA genome. Thicker cell walls inhibit conductance of CO2 from intercellular airspaces to reaction centres of the chloroplasts. Alongside the domestication of modern rice, the few observations made on mesophyll resistance suggest that it has decreased as photosynthetic performance has improved. However, while thicker mesophyll cell walls may impede photosynthesis [54], they have been associated with plants adapted to dry environments [55,56] and might protect against water deficits during low humidity. Cell wall thickness accounts for at most 50% of mesophyll resistance [30,57]. Independent of cell wall thickness, droughtadapted species show increased mesophyll conductance [58,59], most likely as a result of gene control of lipid membrane permeability [60,61]. Competing drought tolerance strategies of increasing cell wall thickness that reduces water loss or increasing mesophyll conductance that facilitates CO2 uptake and improve water use efficiency may be at work. We can report that O. australiensis had increased transpiration rates under hot conditions (>30 ◦ C), indicating that water loss might be accelerated as part of leaf-cooling strategy that has evolved, adding another level of complexity when considering heat and CO2 conductance. A deeper understanding of the processes and genes controlling mesophyll conductance gained through interspecific comparisons [62] might be beneficial in the search for improved water use efficiency in upland rice cultivars. Wild relatives of rice could provide a means for progress once the genetics of anatomical and transport properties have been described and the markers for efficient gene transfer identified (Section 4). Ideally, if mesophyll conductance were inducible according to plant water status as new leaves emerge, carbon gain and water use efficiency could be dynamic and thus better optimised. This might be approached by engineering key functional genes involved in mesophyll conductance to be under the control of inducible transcription factors such as dehydration responsive element binding factors (DREBs) or ABA-responsive elements [63]. 3.3. Photosynthesis Net photosynthesis is a crucial physiological process, being the primary driver of growth and yield [64] and therefore a high priority for breeding programmes. Differences in maximum rate of assimilation have been observed between Oryza species, with O. sativa unsurprisingly having one of the highest rates of photosynthesis [65], without doubt a result of selection for growth rate over a few thousand years. The superior photosynthetic performance of O. sativa coincides with high nitrogen (N) content per unit of leaf, underlining the correlation between leaf N content and photosynthesis across the genus [66,67]. The nitrogen use efficiency of O. sativa does not always exceed that of its wild relatives in spite of millennia of domestication, as demonstrated in comparisons between O. sativa and O. meridionalis [68]. Indeed, wild Oryza

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species from nutrient-poor environments might be a useful source of germplasm for efficient acquisition or phloem re-mobilisation of N and other nutrients such as phosphorus, potassium and micronutrients. Relentless selection of plant species for use as modern, high-yielding crops in wet, fertile soils has probably driven efficient conversion of radiant energy to photoassimilates but not necessarily other efficiencies (e.g. below ground) that might be important as rice-growing extends beyond its traditional range. In general, mechanisms conferring tolerance to abiotic stresses are highly likely to have been eliminated in irrigated, fertilised rice fields. It will be especially important for rice genotypes to incorporate tolerance to high temperatures over the coming decades of more frequent heat waves and constrained water supply, particularly the photosynthetic machinery because it is highly susceptible to heat [69]. Wild species are likely to have heat tolerance genes relating to photosynthesis, as a number of these species evolved in consistently hot habitats (Section 2) with atmospheric maximum temperatures regularly close to 40 ◦ C; plant species from warmer climates normally have higher photosynthesis temperature optima than those from cooler climates [70]. Even though O. sativa shares its AA genome with O. meridionalis, the wild relative has a distinctive tolerance to heat compared to a commercial japonica variety with which it has been compared. An O. meridionalis accession selected from the hot, north of Australia and has a temperature optimum for photosynthesis 3 ◦ C higher than O. sativa (33.7 ◦ C versus 30.6 ◦ C, respectively) [68]. A difference of 3 ◦ C could push many proteins over a stability threshold and lead to reduced carbon acquisition, as observed in O. sativa. Identifying these thresholds in vitro and targeting them with more thermostable proteins in planta must be research priorities, whether they be transcription factors or primary enzymes and transport proteins. The difference in susceptibility to high temperature between rice species has been largely ascribed to a single heat-labile enzyme, Rubisco activase, which facilitates the activity of Rubisco in fixing carbon [68] and transcription factors that control a myriad of genes in rice when exposed to heat stress [71]. Such findings demonstrate the potential impact that single genes, protein complexes and transcription factors can have on entire physiological processes, even when they are complex core processes such as photosynthesis. Recent research has focused on an attempt to achieve rice yield improvement through incorporation of C4 photosynthesis pathways into C3 O. sativa [72]. Although it is unlikely that an Oryza species has evolved a complete C4 pathway, considering the difference in cellular leaf morphology between O. sativa and wild rice (Section 3.1), a possibility exists that some wild Oryza species may have characteristics of Kranz anatomy or even hybrid C3 –C4 intermediate metabolism; this question is currently a major topic of research at the International Rice Research Institute (http://c4rice.irri.org). Oryza coarctata is the only Oryza species known to have C4 bundle sheath traits that approached or matched those found in C4 species [73]. Interestingly, O. coarctata is salt tolerant, raising the question: does O. coarctata achieve salt tolerance, or salt avoidance through greater water use efficiency due to anatomical leaf traits? O. meridionalis was the only other rice species analysed and it had much less C4 similarity. A second study of five Oryza species [74] reported that vein length per leaf, mesophyll thickness and intercellular space volume in rice were intermediate between those of most C3 and C4 grasses, indicative of a CO2 scavenging mechanism on warm-climate grasses. These preliminary findings suggest that the introduction of Kranz anatomy into some rice species may not require radical changes in leaf anatomy. Other Oryza species must be explored in large-scale surveys to determine the extent of ‘C4 -type anatomy’ in wild rice and in which species it is found.

O. sativa O. meridionalis O. australiensis

800

mAbs 324 nm

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600 400 200 0

5

10

15

20

25

30

35

40

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time (min) Fig. 4. Leaf secondary compound profile. HPLC chromatogram of pigments extracted from O. sativa (dark shade), O. meridionalis (medium shade) and O. australiensis (light shade). Tissue was homogenised in 40% ethanol 0.1% acetic acid and extract separated for 45 min using 0.1% formic acid and a gradient of 9–100% acetonitrile, using a reverse phase C18 column.

3.4. Secondary metabolites With nine genomes identified in more than twenty species of Oryza across four continents and diverse climates (Section 2), one would expect high diversity in secondary compounds involved in metabolism and general defence. However, there are only disparate datasets published for wild Oryza species, in spite of the rapidly improving capacity for rapid metabolic profile screening. Striking differences in the profiles of ethanol-soluble leaf extracts have been observed between O. sativa and O. meridionalis and O. australiensis (Fig. 4). While many of the same compounds are found in each species, concentrations of individual compounds differ dramatically. The functional significance of these differences remains obscure although considering that the extracted compounds absorb UV light, they presumably influence the ability of a species to screen harmful UV irradiance. Accordingly, it is interesting in that O. meridionalis has greater tolerance to UVB exposure than O. sativa [75]. Considering UV damage is highly detrimental to plant performance [76] and UV-absorbing pigments protect against such damage [77] screening for highly abundant pigments in wild rice may provide target genes for improving against UV damage. Whether such compounds have a direct role in disease resistance must necessarily be integrated into this line of experimentation by collaboration with plant pathologists [35]. 3.5. Reproduction Crosses between wild germplasm of O. rufipogon and O. sativa have revealed much about the genes that control reproductive development [78–80]. A critical gene appears to be spd6 which controls changes in phenotypic traits associated with seed number and seed weight and consequently increases in grain yield; it is thus proposed that this was a key gene in rice domestication [78–80]. Several of these experiments reveal improved yield (e.g. panicle number and grain weight) in introgression lines, indicating that O. rufipogon has genes that can have a direct benefit to yield. If improvements to a primary domestication trait such as grain yield can be achieved through introgression from the closest of wild relatives such as those in the O. sativa complex, the potential to improve more subtle developmental and adaptive traits that confer tolerance to specific environments becomes plausible. Anthesis is the phenological stage in cereals that manifests the greatest susceptibility to abiotic stress, particularly heat and chilling. Hence anthesis is when the major penalty to yield occurs in less favourable environments such as Africa and Australia. The wild species, Oryza officinalis, mitigates the detrimental impact of high temperature on spikelet fertility by undergoing anthesis early in the day when the air is cooler. This results in greater fertilisation rates

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than an O. sativa cultivar that flowers later in the day [81]. By selecting ecotypes from hotter environments that have erratic rainfall, genes that confer tolerance to abiotic stress at anthesis, or encode for avoidance strategies, might be discovered. The same extreme environments might also yield phenotypes with a range of photoperiod sensitivities and even a perennial growth habit that could tailor them to harsh cultivation systems such as unpredictable rainfall zones [17]. Wild rice species and their hybrids with O. sativa currently make a negligible contribution to world food production in terms of biomass (i.e. starch), they have potential to become very important as a source of inorganic micronutrients as mechanisms of ion accumulation in grain become better understood. Wild rice seed has greater mineral nutrient loads of potassium, magnesium, iron, manganese and selenium and reduced levels of toxic elements such as mercury, lead and cadmium (and arsenic in the case of O. punctata) compared to O. sativa [82]. In our own experiments on Australian O. meridionalis and O. australiensis, key micronutrients were enriched in seed from wild rice plants grown on typical puddled soils in glasshouses, even when considered on a nitrogen basis to correct for low endosperm mass in wild species [48]. In particular, boron, zinc and copper concentrations were at least doubled while nickel, lead and cobalt, for example, were greatly diminished in these wild species. Coupled with 25% higher nitrogen content in seed of wild rice relatives, there is a case for exploiting wild species of Oryza for grain quality. For example, increased protein content of rice seed has been achieved through crosses between O. sativa and O. nivara [83]. In the nineteenth century, Australian Aborigines were reported to mill the seed of a wild rice species as a food source [84]. Which of the two endemic species they used is not reported but it was probably O. meridionalis based on descriptions of the long awns. 3.6. Abiotic stress–response pathways Multiple quantitative trait loci (QTLs) associated with heat response have been identified when O. rufipogon was used as a donor line with a relatively heat-tolerant indica cultivar of O. sativa as the recipient line [85]. Crosses segregated phenotypically into a spectrum of heat sensitivity, with one cross, YIL106, particularly sensitive, as assessed by leaf cell membrane damage, chlorophyll content and soluble sugar concentrations. Such lines will be valuable tools to identify QTLs for tolerance genes and ultimately, the genes that confer stress tolerance. These results also highlight the fact that introgression of wild germplasm, if not targeted, may cause undesirable collateral effects on abiotic stress tolerance. However, hybrids are most useful for making mapping populations (Section 4) and discovery of QTLs. Selecting the appropriate wild rice for improvement through breeding programmes is therefore critical and the use of climate distribution data (Section 2) could greatly facilitate the selection of germplasm with the desirable phenotypic traits. A protein from O. rufipogon, speculated to be involved in metabolic regulation and cell ionic homeostasis is up-regulated after salt application. It provides tolerance to freezing and salt stress when expressed in Arabidopsis [86]. Furthermore, crosses between O. rufipogon and O. sativa have produced introgression lines with improved tolerance to saline conditions, with salt-tolerant hybrids having greater growth rates under the stress condition [87]. However, a hybrid from a less conventional genetic source has now arisen from the breeding programme at the International Rice Research Institute, where a single embryo was rescued from a cross between O. sativa and O. coarctata (Porteresia coarctata). Subsequent backcrossing has secured a fertile, salt-tolerant rice hybrid. The extraordinary salt tolerance of the progeny reflects the tolerance of the Bangladeshi parent line of O. coarctata [88]:

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such approaches will surely accelerate the establishment of abiotic stress tolerance [89]. Where medium-term inundation occurs, the gene SUB1A-1 is responsible for a large proportion of the flood tolerance in O. sativa [90]. Somewhat surprisingly, subsequent experiments showed that this gene confers dehydration tolerance after drought and desubmergence tolerance through control of oxidative damage [91]. This underlines the influence that a few key regulatory genes might have on abiotic stress tolerance. The SUB1A-1 allele is naturally absent in all but a few varieties of the indica sub-species of rice, encouraging one to pursue wild rice relatives that might harbour equally scarce but profoundly important alleles of regulatory genes. For example, two wild rice species, O. rhizomatis and O. eichingeri, which do not have the SUB1A-1 allele, have comparable levels of submergence tolerance [92] indicating that they have evolved alternative signalling pathways. Finding novel stress tolerance pathways may allow for multiple-pathway targeted approaches to improving cultivated rice tolerance to stress, including the paradoxical combination of sequential flooding and dehydration.

4. Introgressing genes from wild rice relatives into O. sativa 4.1. Introgression A vast augmentation of the O. sativa gene pool is conceivable when the genetic diversity of wild relatives is exploited [10,22]. However, the genetic distance from the AA genome of O. sativa is not trivial. The most genetically remote species are O. coarctata, Oryza longiglumis, Oryza meyeriana, O. ridleyi, and O. schlechteri, which include the G, H, J, K and L genomes present in diploid and tetraploid genotypes [37] and Fig. 5. These species can only be used for introgression of novel genes through intervention of labour-intensive techniques, as reported in Section 3.3 for the salt-tolerant hybrid of O. sativa and O. coarctata. The eight wild rice species (including O. sativa) that carry the AA genome can be relatively easily hybridised through conventional breeding practices [17] and are far the most widely collected (Fig. 3). Reflecting this tractable genetic distance, most crosses between wild and domesticated rice species have until now focused on species within the O. sativa complex. In particular, O. rufipogon, widely considered to be the progenitor of O. sativa, has been successfully hybridised with its domesticated counterpart [93] and O. glaberrima has been used in breeding for nematode resistance in O. sativa [94]. There is precedence for more genetically remote crosses, with O. australiensis one of the most distantly related from O. sativa being crossed with O. sativa and providing resistance to the pest brown planthopper [95]. That cross was also achieved through embryo rescue techniques. Transferring genes from wild species that are distantly related will be a painstaking process that is likely to be expedited by use of more sophisticated approaches than conventional breeding. However, O. sativa has been successfully hybridised with all the wild relatives in the genus Oryza, as well as more distant relatives. These are in the first steps towards rice improvement programmes at the International Rice Research Institute (Jena, Pers. Comm.). As for most modern crop species, ongoing natural introgression of wild germplasm into the gene pool has been critical for enrichment of the genetic diversity in rice, providing a palette for intensive selection by farmers over millennia. However, as a means of adapting rice to the changing requirements of modern agriculture, uncontrolled gene flow is impracticable. While wild species of rice are probably more likely to outcross than we observe for modern cultivars of O. sativa [1,96,97], especially those that are perennial [17], rates are too low to ensure efficient transfer of

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Fig. 5. A phylogenetic map of the major wild Oryza species as reported [37]. The thickness of the lineages represents approximate genome size [22,37] while the numbers in brackets are the numbers of wild collections made using databases cited in Fig. 1.

favourable traits when many undesirable genes would be transferred to O. sativa by genetic drag. Improvement of rice in the future through biotechnology will initially involve targeted transfer of Oryza transgenes from O. sativa landraces and wild germplasm into O. sativa, possibly working alongside conventional breeding programmes aimed at identifying critical genes from quantitative trait locus maps. This will raise a further question about whether current commercial rice cultivars and new varieties that will be needed to manage contemporary stresses must draw upon genetics beyond the genus Oryza. There are many candidates for introduction of novel genes from within the sub-family Erhartoideae (Oryza and related species), which diverged from other grasses such as wheat about 46 Mya [98]. These include species of Leersia (e.g. Leersia oryzoides), which are widely distributed, and the monotypic Potomophila parviflora that occupies habitats where there might have been selection for tolerance to submergence and even salinity. Evidence about relatedness from gene duplications [99] suggests that when tolerance genes from these distant species are cloned into O. sativa, they might well be metabolically compatible and produce viable phenotypes. Therefore, when combined with appropriate promoters and RNA regulatory genes, there are real prospects for phenotypic advances in modern rice once target genes are identified. The success of these experiments will depend upon available sequence data, as are being generated for Leersia perrieri, and continuing insights into the physiological processes that constrain performance. For example, genes encoding ion influx and efflux transporters, oxidative stress scavenging enzymes and carbohydrate loading and unloading porters are examples of the targets that are likely to be most productive in phenotype improvement. The discovery of an allele that confers submergence-tolerance [90] in relatively few indica rice varieties underlines the fact that very important tolerance characteristics might be encoded by very rare genes within species. Furthermore, alleles such as SUB1A-1 are now thought more likely to confer multiple tolerances to abiotic stresses, as they operate through core events such as quenching of reactive oxygen species [91]. Reverse genetics targeting genes known to be involved in oxidative stress and hormone responsiveness across the genus Oryza and beyond

might be a powerful application of the Oryza Map Alignment Project [37]. The modelling analysis described in Section 2 is a potential approach to narrow the search for Oryza genes that confer tolerance to abiotic stresses but finer resolution and better phenological information would improve the power of this approach considerably. Finally the importance of the vast and well curated O. sativa germplasm must not be underestimated, with Khaiyan and other landraces helping in the identification of genes for flood tolerance at the germination stage [100]. 4.2. Weediness and escape Even when useful genes are identified and stably introgressed into O. sativa, there are hazards of gene escape which, while not peculiar to rice, are far more likely than in many dryland crops. Rice paddies notoriously have many weeds that thrive in close proximity to the commercial crop under the humid fertile conditions in which rice grows. Particular among these are species such as Echinochloa spp. and Cyperus spp. [101]. However, most hazardous is outcrossing between wild ‘weedy rice’ and domesticated rice. These rice paddy weeds, commonly referred to as ‘red rice’, have diverse genetic origins that include relatedness to O. rufipogon and indica and japonica strains of O. sativa from Asia. Abiotic stress tolerance genes that ‘escaped’ into these red rice populations could become a progressively more serious agronomic burden. Genes that confer an advantage on O. sativa will be selected for if they escape, quickly benefiting weed populations. This will be challenging if not impossible to stop especially as gene flow in weedy populations will be faster with the widespread use of hybrid rice. A recent report suggests that increased atmospheric CO2 concentrations will enhance outcrossing and the flow of genes between rice, through influences on flowering times and reproductive morphological traits [102]. It is therefore a challenge of breeders not only to use the full potential of germplasm of the Oryza genus, but also to limit gene flow between germplasm when it is indiscriminate. How to limit natural introgression between rice genotypes and weedy relatives will be challenging. One proposed mechanism is simply to allow for physical distance between genotypes [15].

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However, a concerted effort to introgress genes from wild Oryza species and more distantly related species through conventional breeding and the use of transgenics calls for a more sophisticated approach than purely physical means to control gene flow in weedy rice. For example, it might require cassettes of genes that confer an advantage on the crop but a fitness penalty for the weeds to which the novel gene has escaped [103].

Acknowledgment We thank Professor Colin Prentice for invaluable advice, support and encouragement for W.H. to participate in this review.

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