Circadian rhythms of hydraulic conductance and growth are enhanced by drought and improve plant performance

Abstract

Circadian rhythms enable plants to anticipate daily environmental variations, resulting in growth oscillations under continuous light. Because plants daily transpire up to 200% of their water content, their water status oscillates from favourable during the night to unfavourable during the day. We show that rhythmic leaf growth under continuous light is observed in plants that experience large alternations of water status during an entrainment period, but is considerably buffered otherwise. Measurements and computer simulations show that this is due to oscillations of plant hydraulic conductance and plasma membrane aquaporin messenger RNA abundance in roots during continuous light. A simulation model suggests that circadian oscillations of root hydraulic conductance contribute to acclimation to water stress by increasing root water uptake, thereby favouring growth and photosynthesis. They have a negative effect in favourable hydraulic conditions. Climate-driven control of root hydraulic conductance therefore improves plant performances in both stressed and non-stressed conditions.

Figure 1. The endogenous rhythm of leaf elongation rate in continuous light is linked to the entrainment period.

(a,e,i) Photosynthetic photon flux density (PPFD). (b,f,j) Vapour pressure deficit (VPD). (c,g,k) Transpiration (Jw). (d,h,l) Leaf elongation rate (LER). (a–d) Entrainment period (EP) in green house at high (red) or low (green) evaporative demand (experiments 11 and 12). (e–h) EP either with low evaporative demand in a growth chamber (green, experiments 22) or high evaporative demand in green house (red and orange, experiments 9 and 8). (i–l) EP in growth chamber at high (red) or low (green) evaporative demands (experiments 20 and 21). Arrows in d indicate the subjective dusks (black) and dawn (blue). Error bars either side of the solid line represent the confidence interval at P<0.05, n≥6 (Supplementary Table 1).

Figure 2. The endogenous rhythm of leaf elongation rate is linked to variations in leaf water potential, plant hydraulic conductance and the expression level of ZmPIP aquaporins in roots.

Experiments 9 and 22, LER presented in Fig. 1, plants with either high (red) or low (green) evaporative demand during EP. (a) Leaf water potential. (b) Plant hydraulic conductance (K_h). (c) Mean expression of 12 PIPs in roots. Values normalized by expression levels of each ZmPIP at 07:00 day 1. Error bars either side of the solid line represent the confidence interval at P<0.05, n=3 in c, n≥15 for other panels (Supplementary Table 1).

Figure 3. The amplitude of LER oscillations increased with water stress and water flux through the plants.

Compared amplitudes during the EP and continuous light for (a) plants introgressed with a genomic region that confers lower sensitivity to water deficit (experiment 2), (b) plants under-expressing the NCED/VP14 gene (experiment 7), (c) plants with common environmental conditions during EP and grown with low (green) or high (red) evaporative demand during continuous light, (d) plants grown in hydroponics at −0.1 MPa during the EP, then at either −0.1 (green) or −0.4 MPa (red) during continuous light (experiment 18). Error bars either side of the solid line represent the confidence interval at P<0.05, n≥8 (Supplementary Table 1). *, ** represent significant difference, t-test at P-values <0.05 and 0.01.

Figure 4. Transcript abundance of core oscillator genes.

Transcript abundance under high and low evaporative demands during EP (red and green lines, respectively). Solid lines represent microarray data (a,b), dotted lines represent qRT–PCR (c–f). (a) GI in roots (b) GI in leaves (c) GI in leaves (d) LHY (e) CCA1 (f) PRR family genes. Circles represent PRR1, triangles represent PRR5, squares represent PRR7. Data represented by green lines in c,e,f is from the study by Khan et al. Error bars represent s.d. n=3. * represents significant difference in a t-test, P<0.05.

Figure 5. The transcript abundance of ZmPIPs aquaporins displayed an endogenous rhythm.

Individual ZmPIPs expressions in roots. Error bars represent confidence interval at P<0.05. Other scenarios of EP for roots and transcript abundance in the growing zone of leaves are presented in Supplementary Fig. 6.

Figure 6. A hydraulic model involving oscillations of hydraulic conductance captures experimental patterns of leaf growth and leaf water potential in experiments 11, 12 and 21.

(a–c) Photosynthetic photon flux density (PPFD) and air vapour pressure deficit (VPD). (d–f) Leaf elongation rate (LER). (g–i) hydraulic conductance controlled by light (red) or circadian movements (blue). (j–l) Water potentials of the xylem (red) and mature cells (green). In d–f, green lines represent measured LER, black lines: simulated LER. a,d,g,j: experiment 11. b,e,h,k: experiment 12. c,f,i,l: experiment 21.

Figure 7. Comparative advantages of high or low oscillation amplitudes of root hydraulic conductance in favourable or unfavourable climatic scenarios for water.

In each scenario, red and green lines represent simulations with high and low amplitudes of water potential. (a,b) Photosynthetic photon flux density (PPFD) and air vapour pressure deficit (VPD). (c,d) Leaf elongation rate (LER). (e,f) Water potential of the rhizosphere. (g,h) Water flux from the bulk soil to the rhizosphere.