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• W4382461567 abstract "Full text Figures and data Side by side Abstract Editor's evaluation eLife digest Introduction Results Discussion Materials and methods Appendix 1 Data availability References Decision letter Author response Article and author information Metrics Abstract While the domestication process has been investigated in many crops, the detailed route of cultivation range expansion and factors governing this process received relatively little attention. Here, using mungbean (Vigna radiata var. radiata) as a test case, we investigated the genomes of more than 1000 accessions to illustrate climatic adaptation’s role in dictating the unique routes of cultivation range expansion. Despite the geographical proximity between South and Central Asia, genetic evidence suggests mungbean cultivation first spread from South Asia to Southeast, East and finally reached Central Asia. Combining evidence from demographic inference, climatic niche modeling, plant morphology, and records from ancient Chinese sources, we showed that the specific route was shaped by the unique combinations of climatic constraints and farmer practices across Asia, which imposed divergent selection favoring higher yield in the south but short-season and more drought-tolerant accessions in the north. Our results suggest that mungbean did not radiate from the domestication center as expected purely under human activity, but instead, the spread of mungbean cultivation is highly constrained by climatic adaptation, echoing the idea that human commensals are more difficult to spread through the south-north axis of continents. Editor's evaluation This is an important interdisciplinary effort, with compelling genetic evidence, that informs on the spread of an important crop. The work will be of broad interest to those studying the domestication and dissemination of cultivated plants. https://doi.org/10.7554/eLife.85725.sa0 Decision letter eLife's review process eLife digest Mungbean, also known as green gram, is an important crop plant in China, India, the Philippines and many other countries across Asia. Archaeological evidence suggests that humans first cultivated mungbeans from wild relatives in India over 4,000 years ago. However, it remains unclear how cultivation has spread to other countries and whether human activity alone dictated the route of the cultivated mungbean’s expansion across Asia, or whether environmental factors, such as climate, also had an impact. To understand how a species of plant has evolved, researchers may collect specimens from the wild or from cultivated areas. Each group of plants of the same species they collect in a given location at a single point in time is known collectively as an accession. Ong et al. used a combination of genome sequencing, computational modelling and plant biology approaches to study more than 1,000 accessions of cultivated mungbean and trace the route of the crop’s expansion across Asia. The data support the archaeological evidence that mungbean cultivation first spread from South Asia to Southeast Asia, then spread northwards to East Asia and afterwards to Central Asia. Computational modelling of local climates and the physical characteristics of different mungbean accessions suggest that the availability of water in the local area likely influenced the route. Specifically, accessions from arid Central Asia were better adapted to drought conditions than accessions from wetter South Asia. However, these drought adaptations decreased the yield of the plants, which may explain why the more drought tolerant accessions have not been widely grown in wetter parts of Asia. This study shows that human activity has not solely dictated where mungbean has been cultivated. Instead, both human activity and the various adaptations accessions evolved in response to their local environments shaped the route the crop took across Asia. In the future these findings may help plant breeders to identify varieties of mungbean and other crops with drought tolerance and other potentially useful traits for agriculture. Introduction Domestication is a process that is cultivated by humans, leading to associated genetic and morphological changes. These changes may be intentional from human selection or unintentional as a result of adaptation to the environments of cultivation (Fuller, 2007). Later, the cultivated plants spread out from their initial geographical range (Meyer and Purugganan, 2013), and elucidating the factors affecting the range expansion of crops is another focus of active research (Gutaker et al., 2020). In the old world, during the process of ‘prehistoric food globalization’ (Jones et al., 2011), crops originated from distinct regions were transported and grown in Eurasia. Archeological evidence has shown that such ‘trans-Eurasian exchange’ had happened by 1500 BC (Liu et al., 2019), and the proposed spread routes from archeological studies were supported by modern genetic evidence especially in rice (Gutaker et al., 2020) and barley (Lister et al., 2018). Interestingly, the spread may accompany genetic changes for the adaptation to novel environments. For example, in barley, variations in the gene Photoperiod-H1 (Ppd-H1) resulting in the non-responsiveness to longer daylengths were likely associated with the historical expansion to high-latitude regions (Jones et al., 2008; Jones et al., 2016). While these mid-latitude cereals have been extensively studied, investigations of crops originated from other climate zones are needed. Using the South Asian (SA) legume mungbean as a test case, here, we investigate how climatic adaptation might affect crop spread route and the evolutionary changes making such spread possible. Mungbean (Vigna radiata [L.] Wilczek var. radiata), also known as green gram, is an important grain legume in Asia (Nair and Schreinemachers, 2020), providing carbohydrates, protein, folate, and iron for local diets and thereby contributing to food security (Kim et al., 2015). Among pulses, mungbean is capable of tolerating moderate drought or heat stress and has a significant role in rainfed agriculture across arid and semiarid areas (Pratap et al., 2019), which are likely to have increased vulnerabilities to climate change. Although there have been studies about the genetic diversity of cultivated and wild mungbean (Ha et al., 2021; Kang et al., 2014; Noble et al., 2018; Sangiri et al., 2007), the evolutionary history of cultivated mungbean after domestication still lacks genetic studies. Existing archeological evidence suggests that South Asia is the probable area of mungbean domestication, and at least two independent domestication events have been suggested, including Maharashtra and the eastern Harappan zone (Fuller and Harvey, 2006). The early archeological records suggest that the selection of large seed sizes occurred in the eastern Harappan zone by the third millennium BC and in Maharashtra, dating to the late second to early first millennium BC (Fuller and Harvey, 2006). This pulse later spread to mainland Southeast Asia and has been reported in southern Thailand dating to the late first millennium BC (Castillo et al., 2016). Further north, the earliest record of mungbean in China was from the book Qimin Yaoshu (齊民要術, 544 AD). While mungbean is also cultivated in Central Asia today, it was not identified in archaeobotanical evidence ranging from several millennium BC to the medieval period (Miller, 1999; Spengler et al., 2018b; Spengler et al., 2017), suggesting later arrival. While the archaeobotanical studies elucidated the route of mungbean cultivation range expansion, researches are still needed to identify the genetic evidence and factors shaping such spread route. A recent genetic study revealed that present-day cultivated mungbeans have the same haplotype in the promoter region, reducing the expression of VrMYB26a (Lin et al., 2022), a candidate gene controlling the important domestication trait, pod shattering, in several Vigna species (Takahashi et al., 2020). This suggests the loss of pod-shattering phenotype in cultivated mungbean may have a common origin and despite the archaeobotanical findings of several independent early cultivations of mungbean in South Asia (Fuller and Harvey, 2006), descendants from one of these cultivation origins might have dominated South Asia before the pan-Asia expansion. Since large regions remain archaeologically unexplored, utilization of genetic data can be a crucial complementation to reconstruct crop evolutionary history. Using seed proteins (Tomooka et al., 1992) and isozymes (Dela Vina and Tomooka, 1994), previous studies proposed two expansion routes out of India, one in the south to Southeast Asia and the other in the north along the silk road to China. While later studies used DNA markers to investigate mungbean population structure (Breria et al., 2020; Gwag et al., 2010; Islam and Blair, 2018; Noble et al., 2018; Sandhu and Singh, 2021; Sangiri et al., 2007), few have examined these hypothesized routes in detail. Therefore, genomic examination of the cultivation rage expansion proposed by archaeobotanical studies and the elucidation of its contributing factors are strongly needed. In this study, we compiled an international effort, reporting a global mungbean diversity panel of more than 1100 accessions derived from (i) the mungbean mini-core collection of the World Vegetable Center (WorldVeg) genebank, (ii) the Australian Diversity Panel (ADP), and (iii) the Vavilov Institute (VIR), which hosts a one-century-old collection enriched with mid-latitude Asian accessions that are underrepresented in other genebanks, many of which were old landraces collected by Nikolai I. Vavilov and his teams in the early 20th century (Burlyaeva et al., 2019). These germplasms harbor a wide range of morphological variations (Figure 1A) and constitute the most comprehensive representation of worldwide mungbean genetic variation. We used this resource to investigate the global history of mungbean after domestication to reveal a spread route highly affected by climatic constraints across Asia, eventually shaping the phenotypic characteristics for local adaptation to distinct environments. Figure 1 with 1 supplement see all Download asset Open asset Diversity of worldwide mungbean. (A) Variation in seed color. (B) ADMIXTURE ancestry coefficients, where accessions were grouped by group assignments (Q≥0.7). (C) Principal component analysis (PCA) plot of 1092 cultivated mungbean accessions. Accessions were colored based on their assignment to four inferred genetic groups (Q≥0.7), while accessions with Q<0.7 were colored gray. (D) Neighbor-joining (NJ) phylogenetic tree of 788 accessions with Q≥0.7 with wild mungbean as outgroup (black color). Results Population structure and spread of mungbean Using DArTseq, we successfully obtained new genotype data of 290 mungbean accessions from VIR Supplementary file 1a. Together with previous data (Breria et al., 2020; Noble et al., 2018), our final set included 1108 samples with 16 wild and 1092 cultivated mungbean. A total of 40,897 SNPs were obtained. Of these, 34,469 bi-allelic SNPs, with a missing rate less than 10%, were mapped on 11 chromosomes and retained for subsequent analyses. The genetic structure was investigated based on the 10,359 LD-pruned SNPs. Principal component analysis (PCA, Figure 1C) showed a triangular pattern of genetic variation among cultivated mungbeans, consistent with previous studies (Breria et al., 2020; Noble et al., 2018; Sokolkova et al., 2020) and ADMIXTURE K=3 (Figure 1B). The geographic distribution of these genetic groups is not random, as these three groups are distributed in South Asia (India and Pakistan), Southeast Asia (Cambodia, Indonesia, Philippines, Thailand, Vietnam, and Taiwan), and more northernly parts of Asia (China, Korea, Japan, Russia, and Central Asia). As K increased, the cross-validation (CV) error decreased a little after K=4 (Figure 1—figure supplement 1), where the north group could be further divided (Figure 1B). Therefore, worldwide diversity of cultivated mungbean could be separated into four major genetic groups corresponding to their geography: SA, Southeast Asian (SEA), East Asian (EA), and Central Asian (CA) groups. Note that the genetic groups were named after the region where most of their members distribute, and exceptions exist. For example, many EA accessions also distribute in Central Asia, and some SEA accessions were found near the eastern and northeastern coasts of India. Throughout this work, we make clear distinction between genetic group names (e.g. SA) and a geographic region (e.g. South Asia). Therefore, unlike any other previous work in this species, this study incorporates global genetic variation among cultivated mungbean of this important crop. Using wild progenitor V. radiata var. sublobata (Wild hereafter) as the outgroup, the accession- (Figure 1D) and population-level (Figure 2A) phylogenies both suggest CA to be genetically closest to EA. The SEA group is more distant, and SA is the most diverged. This relationship is supported by the outgroup f3 tests showing CA shared the highest level of genetic drift with EA, followed by SEA and SA (Supplementary file 1b). Pairwise FST and dxy also give the same conclusion (Figure 2B). Similarly, the f4 tests (Figure 2C) strongly reject the cases where SEA and CA form a clade relative to SA and EA (f4[SA,EA;SEA,CA]=0.016, Z=9.519) or SEA and EA form a clade relative to SA and CA (f4[SA,CA;SEA,EA]=0.021, Z=13.956), again suggesting EA and CA to be closest. With regards to the relationship among Wild, SA, SEA, and EA, f4 tests suggest SEA and EA form a clade relative to Wild and SA (non-significant results in f4[Wild,SA;EA,SEA] but opposite in other combinations). Notably, both TreeMix (Figure 2A) and the f4 test (Figure 2C, f4[SA,SEA;CA,EA]=0.005, Z=6.843) suggest gene flow between SEA and EA. Consistent with archeological evidence of SA domestication, the nucleotide diversity (π) decreased from SA (1.0×10–3) to SEA (7.0×10–4) and EA (5.0×10–4), while the CA group has lowest diversity (3.0×10–4; Figure 2B). Linkage disequilibrium (LD) also decays the fastest in Wild and then the SA group (Figure 2D), followed by other genetic groups. In summary, all analyses are consistent with our proposed order of cultivated mungbean divergence. Figure 2 with 2 supplements see all Download asset Open asset Fine-scale genetic relationship and admixture among four inferred genetic groups. (A) TreeMix topologies with one suggested migration event. Colors on nodes represent support values after 500 bootstraps. (B) Diversity patterns within and between inferred genetic groups as estimated using nucleotide diversity (π in diagonal, where the size of the circle represents the level of π) and population differentiation (FST in upper diagonal and dxy in lower diagonal). (C) f4 statistics. Points represent the mean f4 statistic, and lines are the SE. Only f4 statistics with Z-score>|3| are considered statistically significant. The dashed line denotes f4=0. (D) Linkage disequilibrium (LD) decay. (E) Isolation by distance plot of genetic distance versus geographic distance, with the southern group in red circles and the northern group in blue circles. (F) Relationship between Bio12 (annual precipitation) and nucleotide diversity (π) of the East Asian (EA) genetic group across the east-west axis of Asia. Dot colors represent the annual precipitation of each population. Our proposed demographic history could be confounded by factors such as complex hybridization among groups. For example, SEA and CA might have independently originated from SA and later generated a hybrid population in EA (Figure 2—figure supplement 1A). Other possibilities are that either SEA or CA is the hybrid of other populations (Figure 2—figure supplement 1B and C). We examined these possibilities using f3 statistics for all possible trios among the four groups. None of the tests gave a significantly negative f3 value (Supplementary file 1c), suggesting the lack of a strong alternative model to our proposed relationship among these four groups. Based on the solid relationship among these genetic groups, we used fastsimcoal2 to model their divergence time, allowing population size change and gene flow at all time points (Figure 2—figure supplement 2A–D). According to this model, after initial domestication, the out-of-India event (when other groups diverged from SA) happened about 8.3 thousand generations ago (kga) with 75% parametric bootstrap range between 4.7 and 11.3 kga. Not until more than 5000 generations later (2.7 kga, 75% range 1.1–4.6 kga) did SEA diverge from the common ancestor of present-day EA and CA. CA diverged from EA only very recently (0.2 kga, 75% range 0.1–0.8 kga). Note that the divergence time was estimated in the number of generations, and the much longer growing seasons in the southern parts of Asia may allow more than one cropping season per year (Mishra et al., 2022; Vir et al., 2016). Our results suggest the non-SA accessions have a common origin out of India (otherwise these groups would branch off independently from the SA group). Given this, the phylogenetic relationship (Figure 2A) is consistent with the following hypotheses. (1) The east hypothesis: mungbean expanded eastward and gave rise to the SEA group. This group might initially occupy northeast South Asia and later expanded to Southeast Asia either through the land or maritime route (Castillo et al., 2016; Fuller et al., 2011). The group later expanded northward as EA. EA expanded westward into Central Asia and gave rise to the CA group. (2) The north hypothesis: the group leaving South Asia first entered Central Asia as the EA group. EA expanded eastward into East Asia through the Inner Asian Mountain Corridor (Stevens et al., 2016). The eastern population of EA expanded southward as the SEA group, and later the western population of EA diverged as the CA group. (3) The northeast hypothesis: the group leaving South Asia (through either of the above-mentioned routes) was first successfully cultivated in northern East Asia without previously being established in Southeast Asia or Central Asia. The EA group then diverged southward as SEA and later expanded westward, giving rise to CA. Consistent with this model, the genetic variation of the EA group gradually declines from east to west, accompanied by the gentlest decline of precipitation per unit geographic distance across Asia (Figure 2F). While all three hypotheses are consistent with the phylogeny (Figure 2A), the SEA group originated earlier than EA in the east hypothesis but later in the two other hypotheses. The former case predicts higher nucleotide diversity and faster LD decay in SEA than EA, which is supported by our results (Figure 2B and D). While populations that were established in a region for an extended time could accumulate genetic differentiation, generating patterns of isolation by distance, rapid-spreading populations in newly colonized regions could not (Lee et al., 2017; The 1001 1001 Genomes Consortium, 2016). Using this idea, Mantel’s test revealed a significantly positive correlation between genetic and geographic distances for the SA genetic group (r=0.466, P=0.010), followed by SEA (r=0.252, although not as significant, P=0.069). No such association was found for EA (r=0.030, P=0.142) or CA (r=0.087, P=0.172). In addition, the southern groups (SA and SEA) together (r=0.737, P=0.001) have a much stronger pattern of isolation by distance than the northern groups (EA and CA, r=0.311, P=0.001; Figure 2E). Using Q≥0.5 instead of Q≥0.7 to assign individuals into genetic groups generated results that are largely consistent (Supplementary file 1d). These results are again consistent with the ‘east hypothesis’ that local accessions from the SA and SEA groups were established much earlier than those from EA and CA. Finally, the genetic variation of the EA group is highest in the eastern end and declines westward (Figure 2F). This does not support the north hypothesis where EA first existed in Central Asia and expanded eastward. Environmental differentiation of the inferred genetic groups We further examined the possible causes governing the expansion of mungbean cultivation ranges. For a crop to be successfully cultivated in a new environment, dispersal and adaptation are both needed. Being a crop that has lost the ability of pod shattering, the spread of mungbean was governed by commerce or seed exchange. While barriers such as the Himalayas or Hindu Kush may limit human activity, South and Central Asia was already connected by a complex exchange network linking the north of Hindu Kush, Iran, and the Indus Valley as early as about 4 thousand years ago (kya; Dupuy, 2016; Kohl, 2007; Kohl and Lyonnet, 2008; Lamberg‐Karlovsky, 2002; Lombard, 2020; Lyonnet, 2005), and some sites contain diverse crops originated across Asia (Spengler et al., 2021). Similarly, other ancient land or maritime exchange routes existed among South, Southeast, East, and Central Asia (Stevens et al., 2016). This suggests that mungbean could have been transported from South to Central Asia, but our genetic evidence suggests that the present-day CA group did not descend directly from the SA group. Therefore, we investigated whether climatic adaptation, that is, the inability of mungbean to establish in a geographic region after human-mediated long-range expansion, could be a contributing factor. Multivariate ANOVA (MANOVA) of eight bioclimatic variables (after removing highly-correlated ones; Supplementary file 1e,f) indicated strong differentiation in the environmental niche space of the four genetic groups (Supplementary file 1g,h). PCA of climatic factors clearly reflects geographic structure, where the axis explaining most variation (PC1, 42%) separates north and south groups and is associated with both temperature- and precipitation-related factors (Figure 3A and Supplementary file 1i). Consistent with their geographic distribution, overlaps between EA and CA and between SA and SEA were observed. While these analyses were performed using bioclimatic variables from year-round data, we recognized that summer is the cropping season in the north. Parallel analyses using the temperature and precipitation of May, July, and September yielded similar results (Supplementary file 1j; Figure 3—figure supplement 1). Figure 3 with 5 supplements see all Download asset Open asset Environmental variation among genetic groups of mungbean. (A) Principal component analysis (PCA) of the eight bioclimatic variables. Samples are colored according to four inferred genetic groups as indicated in the legend. (B) Predicted distribution at current climate conditions. Red color indicates high suitability, and blue indicates low suitability. Values between pairs represent niche overlap measured using Schoener’s D, and higher values represent higher overlaps. Abbreviations: SAw: South Asia (west), SAe: South Asia (east); SEA: Southeast Asia; EAe: East Asia (east); EAw: East Asia (west), and CA: Central Asia. (C) Environmental gradient across potential directions of expansion. The value on each arrow indicates a change in annual precipitation per kilometer. The background map is colored according to annual precipitation (Bio12, in mm). Based on the Köppen climate classification (Köppen, 2011), we categorized the Asian mungbean cultivation range into six major climate zones (Figure 3—figure supplement 2): dry hot (BSh and BWh), dry cold (BSk and BWk), temperate dry summer (Csa), tropical savanna (Aw), continental (Dwb and Dfb), and temperate wet summer (Cfa and Cwa). The former three are relatively drier than the latter three zones. While SEA and CA are relatively homogeneous, SA and EA have about half of the samples in the dry and non-dry zones (Figure 3—figure supplement 2). We, therefore, separated SA into SAe and SAw and EA into EAe and EAw, corresponding to the wetter eastern and drier western regions within the SA and EA ranges. Environmental niche modeling revealed distinct suitable regions of these six groups except for CA and EAw, whose geographical ranges largely overlap (Figure 3B). Consistent with PCA, pairwise Schoener’s D values are smallest between the northern and southern groups while largest (suggesting overlaps of niche space) between the eastern and western subsets within north and south (Figure 3B), consistent with PCA that the major axis of climatic difference is between the northern and southern parts of Asia. Analyses using temperature and precipitation from May, July, and September yielded similar results (Figure 3—figure supplement 3). Given a single out-of-India event (Figure 2A), the results suggest it might be easier to first cultivate mungbean in Southeast rather than Central Asia, supporting the east hypothesis. While both temperature and precipitation variables differ strongly between north and south, one should note that these year-round temperature variables do not correctly reflect conditions in the growing seasons. In the north, mungbean is mostly grown in summer where the temperature is close to the south (Figure 3—figure supplement 4A–C). On the other hand, precipitation differs drastically between the north and south, especially for the CA group, where the summer-growing season is the driest of the year (Figure 3—figure supplement 4D). By estimating the regression slope of annual precipitation on geographical distance, we obtained a gradient of precipitation change per unit geographic distance between pairs of genetic groups (Figure 3C). Despite the SA-SEA transect having the steepest gradient (slope = 0.21), the spread from SA to SEA has been accompanied by an increase of precipitation and did not impose drought stress. However, the second highest slope (0.18) is associated with a strong precipitation decrease if the SA group were to disperse to Central Asia. Results from the precipitation of May, July, and September yielded similar conclusion (Figure 3—figure supplement 5). This likely explains why no direct historic spread is observed from South to Central Asia. Trait variation among genetic groups If environmental differences constrained the spread route of mungbean, the currently cultivated mungbean accessions occupying distinct environments should have locally adaptive traits for these environments. Indeed, PCA of four trait categories shows substantial differences among genetic groups (phenology, reproductive output, and size in field trials, as well as plant weight in lab hydroponic systems, Figure 4A). In the field, CA appears to have the shortest time to flowering, the lowest yield in terms of seed size and pod number, and the smallest leaf size (Figure 4B and Supplementary file 1k). On the other hand, SEA accessions maximize seed size, while SA accessions specialize in developing the largest number of pods (Figure 4B). These results suggest that CA has a shorter crop duration, smaller plant size, and less yield, consistent with drought escape phenotypes. This is consistent with the northern short-growing season constrained by temperature and daylength (below), as well as the low precipitation during the short season. Figure 4 with 1 supplement see all Download asset Open asset Quantitative trait differentiation among genetic groups. (A) Principal component analysis (PCA) of four trait categories. (B) Trait variability from common gardens in field experiments. Sample size of SA, SEA, and CA are 18, 17, and 14, respectively. (C) Comparison of QST-FST for four drought-related traits under two environments. FST values (mean, 5%, and 1%) were indicated by black dashed lines. The QST for each trait was colored according to treatment and was calculated as Equation 2 in Materials and methods. Abbreviations: RDW: root dry weight; SDW: shoot dry weight; TDW: total dry weight; RSRDW: root:shoot ratio dry weight; c: control; p: PEG6000. (D) Effect of PEG6000 (–0.6 MPa) on RDW, SDW, TDW, and RSRDW among genetic groups. Sampe size of SA, SEA, and CA are 20, 18, and 14, repectively. Data were expressed as the mean ± SE. Lowercase letters denote significant differences under Tukey’s honestly significant difference test in (B) and (D). In terms of seedling response to drought stress, the QST values of most traits (root, shoot, and whole plant dry weights under control and drought treatments) are higher than the tails of SNP FST, suggesting trait evolution driven by divergent selection (Figure 4C; Figure 4—figure supplement 1). Significant treatment, genetic group, and treatment by group interaction effects were observed except on a few occasions (Table 1). Consistent with field observation, SEA has the largest seedling dry weight (Figure 4D). While simulated drought significantly reduced shoot dry weight (SDW) for all groups, the effect on SEA is especially pronounced (treatment-by-group interaction effect, F2,575 = 23.55, P<0.001, Table 1 and Figure 4D), consistent with its native habitats with abundant water supply (Figure 3—figure supplement 4D and Supplementary file 1l). All groups react to drought in the same way by increasing root:shoot ratio (Figure 4D), suggesting such plastic change may be a strategy to reduce transpiration. Despite the lack of treatment-by-group interaction (F2,575 = 1.39, P>0.05), CA consistently exhibits a significantly higher root:shoot ratio, a phenotype that is potentially adaptive to its native environment of lower water supply (Figure 3—figure supplement 4D and Supplementary file 1l). Table 1 ANOVA F values for the dry weight (mg) of mungbean seedlings across three different genetic groups. Source of vari" @default.
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• W4382461567 title "Author response: Environment as a limiting factor of the historical global spread of mungbean" @default.
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