Root signals and stomatal closure in relation to photosynthesis, chlorophyll a fluorescence and adventitious rooting of flooded tomato plants

Abstract

Background and aims: An investigation was carried out to determine whether stomatal closure in flooded tomato plants (Solanum lycopersicum) results from decreased leaf water potentials (psi(L)), decreased photosynthetic capacity and attendant increases in internal CO(2) (C(i)) or from losses of root function such as cytokinin and gibberellin export.

Methods: Pot-grown plants were flooded when 1 month old. Leaf conductance was measured by diffusion porometry, the efficiency of photosystem II (PSII) was estimated by fluorimetry, and infrared gas analysis was used to determine C(i) and related parameters.

Key results: Flooding starting in the morning closed the stomata and increased psi(L) after a short-lived depression of psi(L). The pattern of closure remained unchanged when psi(;L) depression was avoided by starting flooding at the end rather than at the start of the photoperiod. Raising external CO(2) concentrations by 100 micromol mol(-1) also closed stomata rapidly. Five chlorophyll fluorescence parameters [F(q)'/F(m)', F(q)'/F(v)', F(v)'/F(m)', non-photochemical quenching (NPQ) and F(v)/F(m)] were affected by flooding within 12-36 h and changes were linked to decreased C(i). Closing stomata by applying abscisic acid or increasing external CO(2) substantially reproduced the effects of flooding on chlorophyll fluorescence. The presence of well-aerated adventitious roots partially inhibited stomatal closure of flooded plants. Allowing adventitious roots to form on plants flooded for >3 d promoted some stomatal re-opening. This effect of adventitious roots was not reproduced by foliar applications of benzyl adenine and gibberellic acid.

Conclusions: Stomata of flooded plants did not close in response to short-lived decreases in psi(L) or to increased C(i) resulting from impaired PSII photochemistry. Instead, stomatal closure depressed C(i) and this in turn largely explained subsequent changes in chlorophyll fluorescence parameters. Stomatal opening was promoted by the presence of well-aerated adventitious roots, implying that loss of function of root signalling contributes to closing of stomata during flooding. The possibility that this involves inhibition of cytokinin or gibberellin export was not well supported.

Fig. 1.

Effects of flooding the soil for up to 83 h on (A) leaf water potential and (B) leaf conductance of the third and fourth oldest leaves of 1-month-old tomato plants. Flooding was started either at the start or at the end of a photoperiod. Linear correlation between leaf conductance and leaf water potential is given in (C). Each point in (A) and (B) represents the mean of seven replicates. Vertical lines are LSDs at P = 0·05. Black boxes on the x-axis indicate dark periods.

Fig. 2.

The effect of soil flooding for up to 52 h on (A) leaf conductance of the fifth oldest leaf and (B) whole-plant transpiration rates in 1-month-old tomato plants. Each point represents the mean of eight replicates. Vertical lines are LSDs at P = 0·05. Black boxes on the x-axis indicate dark periods.

Fig. 3.

The effect of soil flooding for up to 52 h on (A) quantum efficiency of PSII photochemistry (F_q′/F_m′), (B) photochemical fluorescence quenching (F_q′/F_v′), (C) the operating efficiency of PSII photochemistry (F_v′/F_m′), (D) non-photochemical fluorescence quenching (NPQ) and (E) maximum quantum efficiency of PSII photochemistry (F_v/F_m). Plants were dark-adapted for approx. 20 min prior to measurement of F₀ and F_m to estimate NPQ and F_v/F_m at the end of each photoperiod. Each point represents a mean of 24 replicate measurements made on the fifth oldest leaves of eight 1-month-old plants per treatment. Vertical lines are LSDs at P = 0·05. Black boxes on the x-axis indicate dark periods.

Fig. 4.

Linear correlations between leaf conductances and (A) quantum efficiency of PSII photochemistry (F_q′/F_m′) or (B) maximum quantum efficiency of PSII photochemistry (F_v/F_m) during 3 d flooding of 1-month-old tomato plants. Points are from paired individual readings taken over 3 d of flooding. R is the correlation coefficient, and dashed lines show the confidence range at P = 0·05.

Fig. 5.

Effect of reducing C_a by 100 µmol mol⁻¹ on (A) quantum efficiency of PSII photochemistry (F_q′/F_m′), (B) the operating efficiency of PSII photochemistry (F_v′/F_m′), (C) photochemical fluorescence quenching (F_q′/F_v′), (D) non-photochemical fluorescence quenching (NPQ) and (E) maximum quantum efficiency of PSII photochemistry (F_v/F_m) of well-drained tomato plants. Plants were dark-adapted for at least 20 min prior to measurement of F₀ and F_m to estimate NPQ and F_v/F_m. Each point represents the mean of 24 replicate measurements made on the fifth oldest leaves of eight 1-month-old plants per treatment. Vertical lines are LSDs at P = 0·05. Black boxes on the x-axis indicate dark periods.

Fig. 6.

Effect of retaining or removing a pre-formed and well-aerated adventitious root system (AR) on leaf conductances of the third oldest leaves of flooded and well-drained 1-month-old tomato plants.