Hydraulics matter : investigating key hydraulic traits related to drought resistance in wheat (Triticum sp.)

Global crop production is threatened by the increasing periods of water stress arising from warmer and drier conditions predicted under climate change. Developing crop cultivars that will have the capacity to maintain a high productivity under drier environmental conditions has become necessary to face the challenge of climate change while preserving a global food security. There is a substantial body of work on the genetic determinants of ‘standard’ functional traits (i.e. morpho-anatomical traits) underlying drought resistance in crops, whereas ‘mechanistic’ traits (i.e. physiological and hydraulic traits) remain understudied in cereals and are poorly considered in breeding programs. It is essential to better characterise the key physiological traits related to drought response in crops as they reflect plant ability to maintain functioning and integrity under water limitation. In particular, the hydraulic system plays a major role in plant growth and productivity by delivering water to all plant organs and can be damaged during drought. Water movement from roots to leaves is driven by a xylem pressure gradient generated by leaf transpiration, that enables photosynthesis and growth. As conditions get drier, the xylem pressure becomes more negative causing a decline in plant productivity as plant transpiration is reduced (i.e. stomatal closure) to preserve water. Under a prolonged water stress, the xylem pressure can reach a threshold triggering xylem cavitation (i.e. air entry and propagation in the xylem vessels) that induces irreversible damage to the hydraulic system and can ultimately lead to plant death.

In this dissertation I focused on the common wheat (Triticum aestivum), a major cereal crop grown worldwide and a major primary source of food for humans. Wheat production is already affected by the changing climate and grain yield has reached a plateau in the most productive regions of the world. It is likely that wheat hydraulic system is damaged after experiencing drought, therefore assessing the extent to which the vascular system can withstand drier conditions would provide significant information regarding the capacity of wheat to cope with climate change

The emergence of methods allowing direct visualisation of xylem cavitation during dehydration (i.e. the optical technique, the X-ray micro-computed tomography) provides opportunities to better understand the key physiological traits involved in drought resistance in wheat. In this context, the objectives of my thesis were to investigate the hydraulic response of T. aestivum under a water stress and how it relates to other physiological mechanisms; and to assess the role of domestication (i.e. interspecific variability) and breeding (i.e. intervarietal variability) in the evolution of the hydraulic response to drought in wheat.

In Chapter 2, I investigate the changes in leaf hydraulic conductance (K_leaf) and stomatal conductance (g_s) during a water stress. The decline in g_s under water limitation is well documented in vascular plants, however it is still not clear whether changes in the soil water availability or a reduction in K_leaf drives stomatal closure. In water stressed seedling_s of T. aestivum, g_s declined concomitantly with K_leaf at leaf turgor loss. Under such moderate water stress, neither xylem cavitation nor xylem deformation were observed in wheat, thus the decline in K_leaf was attributed to changes in the hydraulic conductance of extra-xylary tissues. Despite its sensitivity to dehydration, the magnitude of Kleaf was too high to be responsible for stomatal closure. T. aestivum exhibited a narrow stomatal safety margin (i.e. the difference of xylem pressure between complete stomatal closure and the onset of xylem cavitation) putting it at risk of hydraulic dysfunction under drier conditions. These results emphasize the need to better understand the hydraulic response of wheat under water stress and to determine how drought resistance evolved during recent wheat history under human actions

In Chapter 3, I explore the effect of domestication on the evolution of drought response across wheat phylogeny, including both wild and cultivated species. Based on my study of 15 species and subspecies of the genera Triticum and Aegilops, I conclude that human actions to enhance production, and particularly domestication, came at a cost of a more drought-sensitive hydraulic system. My results show that leaf vulnerability to xylem cavitation (P50) varies widely through wheat phylogeny and wild progenitors are more resistant to hydraulic damage during a water stress than their cultivated progeny. Moreover, the P50 increases with the ploidy level, hence the hexaploid T. aestivum is more vulnerable to hydraulic dysfunction during drought than its diploid progenitors. Interestingly, the dynamic of leaf shrinkage during dehydration (which reflects changes in plant water status) is preserved within wheat phylogeny. Together, these findings expose a shift from a safer hydraulic strategy in wild progenitors to a more productive strategy in cultivated wheats. Considering that selective breeding led to a genetic bottleneck in modern wheat, I question whether the intraspecific variability in drought resistance of Triticum aestivum is sufficient to be used as a genetic source for breeding cultivars for the future.

In Chapter 4, I show that there is genetic variation in the xylem vulnerability to cavitation between recent cultivars bred for enhanced productivity in local environments. However, contrary to our expectations, cultivars bred for drier environments were not necessarily more resistant to xylem cavitation than cultivars grown in a temperate climate, which underline the need to better understand how resistance to xylem cavitation can be selected to produce ‘drought-resistant’ cultivars.

This thesis presents a novel insight into a key hydraulic trait involved in drought response of the common wheat, a major crop largely understudied and whose global production is threatened by climate change. Using cutting-edge technologies to visualise xylem under water stress provides a great opportunity to investigate the resistance of the vascular system towards water stress and to evaluate how it evolved under human actions. A greater understanding of the hydraulic response of crops under water limitation will contribute to better understand their drought resistance and could improve breeding programs.