Unravelling the diversity in water usage among wild banana species in response to vapour pressure deficit

Abstract

The rise in global temperature is not only affecting plant functioning directly, but is also increasing air vapour pressure deficit (VPD). The yield of banana is heavily affected by water deficit but so far breeding programs have never addressed the issue of water deficit caused by high VPD. A reduction in transpiration at high VPD has been suggested as a key drought tolerance breeding trait to avoid excessive water loss, hydraulic failure and to increase water use efficiency. In this study, stomatal and transpiration responses under increasing VPD at the leaf and whole-plant level of 8 wild banana (sub)species were evaluated, displaying significant differences in stomatal reactivity. Three different phenotypic groups were identified under increasing VPD. While (sub)species of group III maintained high transpiration rates under increasing VPD, M. acuminata ssp. errans (group I), M. acuminata ssp. zebrina (group II) and M. balbisiana (group II) showed the highest transpiration rate limitations to increasing VPD. In contrast to group I, group II only showed strong reductions at high VPD levels, limiting the cost of reduced photosynthesis and strongly increasing their water use efficiency. M. acuminata ssp. zebrina and M. balbisiana thus show the most favourable responses. This study provides a basis for the identification of potential parent material in gene banks for breeding future-proof bananas that cope better with lack of water.

Keywords: breeding; drought tolerance; stomatal conductance; transpiration; vapour pressure deficit; water use efficiency; wild banana species.

Figure 1

Quantification of the transpiration reduction (ϕ_E) according to Franks et al (1999). and Ryan et al. (2016). A linear regression was fitted through the transpiration rate at the first two air-to-leaf vapour pressure deficit (VPD_leaf) levels. This linear regression was extrapolated (dashed line) to estimate the transpiration rate (E_pred) at VPD_leaf of 2.69, 3.28 and 3.87 kPa. E_pred was then compared to the measured transpiration rate (E_meas) to calculate ϕ_E (Eq. 1).

Figure 2

Three phenotypic groups (I, II, III) were defined by k-means clustering based on the stomatal reduction, transpiration reduction and photosynthetic limitation under increasing VPD (see variables in Table 2 ). Both variables measured by leaf gas exchange and whole-plant transpiration were included. Lines and regions represent the three phenotypic groups from k-means clustering plotted along the first two principal components ( Table 2 ). The first principal component was mainly determined by the limitation of photosynthetic rate at high VPDs and the transpiration reduction at leaf and whole-plant level. Important variables in the second principal component were the slope before the breakpoint in transpiration rate with increasing VPD and the stomatal reduction.

Figure 3

Gas exchange response to step-increases in leaf-to-air vapour pressure deficit (VPD_leaf) for 9 wild banana accessions. Steady-state response of (A) stomatal conductance (g_s), (B) transpiration rate (E_rate), (C) photosynthetic rate (A), (D) intrinsic water use efficiency (_iWUE) to increasing VPD_leaf. Data represent mean ± se values after 60 min at a specific VPD_leaf level (n=3-7). Significance is shown in Table A.1 .

Figure 4

Transpiration rate response of 9 wild banana accessions to step-increases in leaf-to-air vapour pressure deficit (VPD_leaf). A significant breakpoint in transpiration rate was identified for all accessions (P-value Davies Test < 0.05). Solid grey lines represent slopes of the modelled segmented response. Grey point and dashed grey line represent the breakpoint in transpiration rate and the VPD_leaf of the breakpoint. Data represent mean ± se values after 60 min at a specific VPD_leaf level (n=3-7).

Figure 5

Slopes and breakpoints of the segmented transpiration rate response to step-increases in leaf-to-air vapour pressure deficit (VPD_leaf). (A) Relation between the breakpoint in transpiration rate and the slope before the breakpoint. (B) Relation between the breakpoint in transpiration rate and the slope after the breakpoint. Three groups (I, II, III) were defined by k-means clustering and are represented by black lines connecting the included accessions. All segmented responses were significant (P < 0.05). Data represent the optimal estimated value ± se. (n=3-7).

Figure 6

Transpiration reduction (ϕ_E) and limitation of photosynthetic rate (A) with increasing leaf-to-air vapour pressure deficit (VPD_leaf). (A) ϕ_E in response to increasing VPD_leaf. ϕ_E was determined as shown in Eq. 1. (B) Limitation of A in response to increasing VPD_leaf. The limitation of A was determined as shown in Eq. 2. Data represent mean ± se. (n=3-7). Significance is shown in Tables A.2 , A.3 .

Figure 7

Stomatal reduction (ϕ_stom) in relation to the maximum observed stomatal conductance (max g_s). The ϕ_stom and max g_s were significantly correlated (R² = 0.88, P < 0.001). Data represent mean ± se (n=3-7). Significance is shown in Table A.4 .

Figure 8

Whole-plant transpiration rate (E_rate) response to step-increases in air vapour pressure deficit (VPD) for 9 wild banana accessions. Note that VPD values slightly differed between accessions depending on the maximal drying capacity of the growth chamber. Data represent mean ± se values after 60 min at a specific VPD level (n=4-8). Significance is shown in Table A.5 .

Figure 9

Whole-plant transpiration rate (E_rate) response of 9 wild banana accessions to step-increases in air vapour pressure deficit (VPD). A significant breakpoint in transpiration rate was identified for all accessions (P-value Davies Test < 0.05). Solid grey lines represent slopes of the modelled segmented response. Grey point and dashed grey line represent the breakpoint in transpiration rate and the VPD of the breakpoint. Data represent mean ± se (n=4-8).

Figure 10

Slopes and breakpoints of the segmented whole-plant transpiration rate (E_rate) response to step-increases in air vapour pressure deficit (VPD). (A) Relation between the breakpoint in whole-plant transpiration rate and the slope before the breakpoint. (B) Relation between the breakpoint in whole-plant transpiration rate and the slope after the breakpoint. Three groups (I, II, III) were defined by k-means clustering and are represented by black lines connecting the included accessions. All segmented responses were significant (P < 0.05). Data represent the optimal estimated value ± se (n = 4-8).

Figure 11

Transpiration reduction measured at whole-plant level (ϕ_E, whole-plant) at VPD 2.64 kPa in relation to the transpiration reduction measured at leaf level (ϕ_E, leaf level) at VPDleaf 2.69 kPa. The ϕ_E at leaf and whole-plant level were significantly correlated (R² = 0.52, P < 0.05). Data represent mean ± se (n=4-8). Significant differences between accessions or groups are indicated in Tables A.2 , A.6 .