The genetic basis of transpiration sensitivity to vapor pressure deficit in wheat

Abstract

Genetic manipulation of whole-plant transpiration rate (TR) response to increasing atmospheric vapor pressure deficit (VPD) is a promising approach for crop adaptation to various drought regimes under current and future climates. Genotypes with a non-linear TR response to VPD are expected to achieve yield gains under terminal drought, thanks to a water conservation strategy, while those with a linear response exhibit a consumptive strategy that is more adequate for well-watered or transient-drought environments. In wheat, previous efforts indicated that TR has a genetic basis under naturally fluctuating conditions, but because TR is responsive to variation in temperature, photosynthetically active radiation, and evaporative demand, the genetic basis of its response VPD per se has never been isolated. To address this, we developed a controlled-environment gravimetric phenotyping approach where we imposed VPD regimes independent from other confounding environmental variables. We screened three nested association mapping populations totaling 150 lines, three times over a 3-year period. The resulting dataset, based on phenotyping nearly 1400 plants, enabled constructing 63-point response curves for each genotype, which were subjected to a genome-wide association study. The analysis revealed a hotspot for TR response to VPD on chromosome 5A, with SNPs explaining up to 17% of the phenotypic variance. The key SNPs were found in haploblocks that are enriched in membrane-associated genes, consistent with the hypothesized physiological determinants of the trait. These results indicate a promising potential for identifying new alleles and designing next-gen wheat cultivars that are better adapted to current and future drought regimes.

FIGURE 1

Examples of whole‐plant transpiration rate (TR) response curves to temperature‐independent increases in atmospheric vapor pressure deficit (VPD) for six lines selected from the three families (two lines per family). Panels A–B, C–D, and E–F represent responses of two genotypes from FAM14 (14–004 and 14–056), FAM22 (22–025 and 22–045) and FAM24 (24–034 and 24–048), respectively, including data from all three independent experiments. Linear (slope) and segmented (Slope1, Slope2, VPD_BP) regression parameters, along with their coefficients of determination (R²) are indicated.

FIGURE 2

Variation in best fits (linear vs. segmented, panel A) and their parameters (panels B–E) for transpiration rate (TR) response curves to increasing vapor pressure deficit (VPD) across the three nested association mapping (NAM) families. In panels B–E, horizontal segments (blue and orange for linear and segmented fits, respectively) reflect the range, while the circle's position indicates the median value for the parameter of interest. The letter n reflects the number of genotypes best described by a linear or segmented response in each family. Parameters slope, Slope1, Slope2 and VPD_BP are fully described in the materials and methods.

FIGURE 3

Frequency distribution of the four TR traits. Panels A, B, C, and D represent data for TR_1.5, TR_2.0. TR_2.5 and TR_3.0 respectively. In each panel, the values of four parents are highlighted by the gray arrows. Broad sense repeatability (r) values are reported in each panel.

FIGURE 4

Correlation matrix between the traits considered in the analysis. Positive and negative correlations are indicated as shades of blue and red. The color, shade, and size of the circles are respectively proportional to the direction and value of the correlation coefficients, as indicated by the scale on the right‐hand side of the figure.

FIGURE 5

Scatter plot of the first three principal components generated from the genetic data of the 150 lines used in this study. The three NAM families are color‐coded as outlined in the insert.

FIGURE 6

Genetic map of statistically significant markers associated with the studied traits. Each point in the map represents the marker's physical position in mega base pairs, with colors corresponding to different traits. Only those chromosomes where significant markers are found are shown (10 out of 21 wheat chromosomes).

FIGURE 7

Manhattan plots showing significant SNPs associated with traits controlling transpiration rate (TR) response to increasing vapor pressure deficit (VPD). Results are shown based on two genome‐wide association models, N (left) and K (right) for TR_1.5 (A, B), TR_2.0 (C, D), TR_2.5 (E, F) and TR_3.0 (G, H). In each panel (except G), the horizontal line indicates the threshold level above which SNPs are declared as significantly associated with the trait with an FDR of 0.05.

FIGURE 8

Gene ontology term distribution in haploblocks where three major SNPs associated with TR response to VPD are located on chromosomes 5A (A, B) and 5C