Environment as a limiting factor of the historical global spread of mungbean

  1. Pei-Wen Ong
  2. Ya-Ping Lin
  3. Hung-Wei Chen
  4. Cheng-Yu Lo
  5. Marina Burlyaeva
  6. Thomas Noble
  7. Ramakrishnan Madhavan Nair
  8. Roland Schafleitner
  9. Margarita Vishnyakova
  10. Eric Bishop-von-Wettberg
  11. Maria Samsonova
  12. Sergey Nuzhdin
  13. Chau-Ti Ting
  14. Cheng-Ruei Lee  Is a corresponding author
  1. Institute of Plant Biology, National Taiwan University, Taiwan
  2. Institute of Ecology and Evolutionary Biology, National Taiwan University, Taiwan
  3. World Vegetable Center, Taiwan
  4. N.I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR), Russian Federation
  5. Department of Agriculture and Fisheries, Australia
  6. World Vegetable Center, South and Central Asia, India
  7. Department of Plant and Soil Science and Gund Institute for the Environment, University of Vermont, United States
  8. Department of Applied Mathematics, Peter the Great St. Petersburg Polytechnic University, Russian Federation
  9. University of Southern California, United States
  10. Department of Life Science, National Taiwan University, Taiwan
5 figures, 3 tables and 2 additional files

Figures

Figure 1 with 1 supplement
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).

Figure 1—figure supplement 1
Cross-validation (CV) errors of ADMIXTURE.

Means of CV errors were calculated based on K values ranging 1–10 with 10 independent runs.

Figure 2 with 2 supplements
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.

Figure 2—figure supplement 1
Schematic representation to investigate presence of admixture in a target population from two source populations using admixture f3 statistic.

(A) f3(EA; SEA, CA), (B) f3(SEA; SA, EA), and (C) f3(CA; EA, SA). Colored circles indicate the geographic area occupied by distinct genetic groups. Arrows indicates the possible direction of expansion and admixture among populations.

Figure 2—figure supplement 2
Estimates of divergence time and inferred mungbean movement over time across Asia.

The histograms of the divergence times represent (A) split time between South Asian (SA) and (Southeast Asian [SEA],[East Asian [EA], Central Asian [CA]]), (B) split time between SEA and (EA,CA), and (C) split time between EA and CA. (D) Geographic distribution of mungbean accessions and proposed mungbean spread routes. Exact locations for Vavilov Institute (VIR) accessions (filled circle) and Global Biodiversity Information Facility (GBIF) records (filled triangle) are provided. Each accession was colored the same as an inferred genetic group using ADMIXTURE in Figure 1. Arrow indicates the possible expansion directions. The map was shaded as a gray color representing altitude (meters above sea level).

Figure 3 with 5 supplements
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).

Figure 3—figure supplement 1
Principal component analysis (PCA) of the growing season climatic data including temperature and precipitation of May, July, and September.

Samples are colored according to four inferred genetic groups, as indicated in the legend.

Figure 3—figure supplement 2
The distribution of accessions in major climate zones according to the Köppen climate classification (Köppen, 2011).
Figure 3—figure supplement 3
Predicted distributions of six groups based on monthly temperature and precipitation (May, July, and September) during the summer growing season.

Red color indicates high suitability, and blue indicates low suitability. Values between groups represent niche overlap measured using Schoener’s D. Abbreviations: SAw: South Asia (west), SAe: South Asia (east); SEA: Southeast Asia; EAe: East Asia (east); EAw: East Asia (west); and CA: Central Asia.

Figure 3—figure supplement 4
Monthly temperature and precipitation variations among the four genetic groups.

Monthly (A) maximum temperature, (B) minimum temperature, (C) mean temperature, and (D) precipitation were computed based on median value among all accessions of a group. Genetic group were colored the same as in Figure 1.

Figure 3—figure supplement 5
Environmental gradient across Asia.

The value on each arrow indicates a change in mean precipitation for May, July, and September (growth season) per kilometer. The background map is colored according to summer precipitation (Bio18, precipitation of warmest quarter, in mm).

Figure 4 with 1 supplement
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).

Figure 4—figure supplement 1
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 1 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.

Author response image 1

Tables

Table 1
ANOVA F values for the dry weight (mg) of mungbean seedlings across three different genetic groups.
Source of variationDegrees of freedom (df)Root dry weightShoot dry weightTotal dry weightRoot:shoot ratio dry weight
Treatment12.65n.s.133.26***72.26***978.76***
Genetic group260.63***79.62***76.54***13.27***
Treatment × Genetic group23.29*23.55***17.79***1.39n.s.
  1. *P<0.05 and ***P<0.001; n.s. non-significant.

Author response table 1
DivergenceMutation 1e-8Mutation 2e-8
SA vs. (SEA,(EA,CA))4.7 to 11.3 kga5.6 to 11.3 kga
SEA vs. (EA,CA)1.1 to 4.6 kga1.3 to 5.4 kga
EA vs. CA0.1 to 0.8 kga0.1 to 0.5 kga
Author response table 2
TitleReferenceBioProjectStatus
Australian mungbean diversity panel collection – DArTseqNoble et al., 2018PRJNA963182Available
World Vegetable Center Mini Core Collection – DartSeqBreria et al., 2020PRJNA645721Available
Vavilov Institute (VIR) mungbean collection – DArTseqPRJNA809503Release immediately following publication

Additional files

MDAR checklist
https://cdn.elifesciences.org/articles/85725/elife-85725-mdarchecklist1-v2.pdf
Supplementary file 1

History of mungbean spread: genetic, environment, and traits data.

(a) Mungbean accessions from Vavilov Institute (VIR) collection. (b) Outgroup f3 statistics among all possible combinations of genetic group pairs. (c) Admixture f3 statistics among all possible population trios. (d) Mantel tests for isolation by distance of inferred genetic group (Q≥0.5). (e) Description of bioclimatic variables used in ecological niche modeling. (f) Pearson’s correlation coefficient between pairs of bioclimatic variables (denoted in lower triangle). (g) Comparison of bioclimatic variables among the four genetic groups analyzed with multivariate ANOVA (MANOVA). (h) Summary of ANOVA for bioclimatic variables. (i) Correlation between eight bioclimatic variables and climatic PC axes 1–4. (j) Comparison of summer growing season data including temperature and precipitation of May, July, and September among the four genetic groups analyzed with MANOVA. (k) ANOVA table for all evaluated field traits (phenology, reproduction, and size) as well as drought-related traits. (l) Mean of eight bioclimatic variables of the genetic groups

https://cdn.elifesciences.org/articles/85725/elife-85725-supp1-v2.docx

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  1. Pei-Wen Ong
  2. Ya-Ping Lin
  3. Hung-Wei Chen
  4. Cheng-Yu Lo
  5. Marina Burlyaeva
  6. Thomas Noble
  7. Ramakrishnan Madhavan Nair
  8. Roland Schafleitner
  9. Margarita Vishnyakova
  10. Eric Bishop-von-Wettberg
  11. Maria Samsonova
  12. Sergey Nuzhdin
  13. Chau-Ti Ting
  14. Cheng-Ruei Lee
(2023)
Environment as a limiting factor of the historical global spread of mungbean
eLife 12:e85725.
https://doi.org/10.7554/eLife.85725