Nightly business: Links between daytime canopy conductance, nocturnal transpiration and its circadian control illuminate physiological trade-offs in maize

Daytime canopy traits have been shown to be related to crop fitness and productivity. Particularly, decreased canopy conductance under high evaporative demand has been linked to increased drought tolerance and improved yields in maize. However, the extent of natural variation of this trait in maize remains largely unknown. Furthermore, nocturnal canopy traits, and particularly nighttime transpiration rate (TRN), remain undocumented in maize. In this regard, recent evidence in trees suggests a non-negligible TRN and a coupling between nighttime water use and daytime canopy conductance that is under the control of the circadian clock. This defines a framework for the 'anticipative hypothesis' which posits that such regulation enhances daytime water-use efficiency. Using a novel gravimetric phenotyping approach deployed on parents of a popular maize nested association mapping panel, here we show that while they displayed variation in maximal conductance, none of these lines exhibited the water-saving decrease in daytime canopy conductance, indicating that this is likely a rare trait in maize. In contrast, significant genetic diversity in TRN was found, with values that were up to 18% of daytime TR, indicating a potential involvement of TRN in maize water use and therefore drought tolerance. Importantly, TRN measured under the well-watered conditions of this study was found to be positively correlated with daytime canopy conductance and to lower leaf construction costs (i.e., increase in specific leaf area, SLA), with no relationship with leaf area. This association was found to be partly mediated by a pre-dawn, genotype-dependent circadian increase in TRN, which strongly correlated with whole-night TRN and SLA but not with leaf area. Collectively, those findings indicate that in maize, there is an untapped variation in TRN with potential implications on plant productivity and fitness, particularly in drought-prone environments.