Functional Optimization And Tissue Spatial Arrangement In Aboveground Hydraulic System Of Basal Angiosperms With A Focus On Malagasy Magnoliids

Multiple structural and functional innovations accompanied the evolution of angiosperms.Vessel innovation allows the xylem to transport water at a faster rate than tracheids.The xylem parenchyma contributes to the dynamic responses of the xylem to the variations in the environment.Thick wall fibers help the mechanical strength of the stem.Dense leaf venation increases the leaf hydraulic conductance.It is a non-exhaustive list of innovations that helps the performance of angiosperms.Optimal tissue construction requires strategical biomass,space and energy investment.The isolated improvement of a function may not provide a significant improvement in the growth or survival of an individual unless it is coordinated with other functions.Instead,it may depreciate the ability of the tissue/ organ/plant to perform other functions.Earlier researches have uncovered multiple coordinations and trade-offs between the aforementioned functional traits.Space,energy and biomass limitations generally accentuate these trade-offs.Nevertheless,functional tradeoffs and trait coordination are often weak.The weakness of the relationships between two functions may suggest that other variables eventually help to optimize or depreciate both functions.Until know,our understanding on the link between structural innovations,functional optimization and ecological dominance of angiosperms is still limited.Basal angiosperms,including magnoliids,evolved separately from the eudicots,and most did not reach the functional performance of more derived angiosperms.The water transport efficiency of magnoliid species is generally low,and the xylem is vulnerable to embolism.The leaf vein density,stomatal conductance,and photosynthetic rate of magnoliids are still low.Such features make of magnoliids a suitable clade for the study of the contribution of structural innovations found in angiosperm on the functional optimization of their organs.Our research is focused on magnoliids from Madagascar.We aimed to identify the strategies that optimize the functional performance of organs and weaken the tradeoff between functional traits.We speculate that the spatial arrangement of tissues can modulate these relationships.Spatial arrangement is expected to be an inexpensive way to improve the functionality of a given tissue.First,we analyzed the relationships between hydraulic efficiency-safety optimization and stem xylem anatomy.We aimed to determine whether the fraction and arrangement of parenchyma tissue in the secondary xylem influences the hydraulic efficiency-safety trade-off in basal angiosperms.We examined the xylem anatomical structure and hydraulic functioning of 28 woody species of magnoliids in a tropical rainforest of Madagascar.We reported,for the first time,quantitative measurements that support the relationship between vessel-to-xylem parenchyma connectivity and the hydraulic efficiency-safety trade-off.We hypothesized that considering the multiple benefits that xylem parenchyma provides,investment in xylem parenchyma would not negatively affect hydraulic conductivity,embolism resistance,or wood density,despite xylem space limitations.We found that at a given conduit lumen fraction,species with higher axial parenchyma fraction(APf)had significantly higher hydraulic conductivity.No significant correlation was found between the axial parenchyma fraction and wood density.On the contrary,species with a higher ray parenchyma fraction,despite having larger vessel fraction were also more vulnerable to embolism.In addition,their wood was lighter.Challenging the space limitation hypothesis by Bittencourt et al.(2016),we expected that species with higher axial and ray parenchyma fractions would be hydraulically optimized.For that,we defined a metric – the distance of species from the trade-off limit – that quantifies the co-optimization of hydraulic efficiency and safety.We found that hydraulically optimized efficiency-safety was accompanied by higher APf and lower ray parenchyma fraction(RPf).Similarly,we expected that species with higher connectivity between vessels and xylem parenchyma would be closer to the limit line.The connectivity between vessels and xylem parenchyma was quantified by the relative fraction of the vessel perimeter that is in contact with the xylem parenchyma.The axial parenchyma fraction only explained 50% of the variance in the vessel-to-axial parenchyma connectivity.Nonetheless,its contribution to the hydraulic optimization metric was similar to the contribution of the xylem parenchyma fraction.Our results provide evidence that axial parenchyma fraction and paratracheal arrangement are associated with both enhanced hydraulic efficiency and optimized hydraulic efficiency and safety.Then,we analyzed the leaf structure and water regime,and aimed to characterize the contribution of vein arrangement to the leaf desiccation tolerance,capacitance,construction cost,and stomatal design across all 30 studied magnoliids – the 28 species used the study of the branch traits and two other herbaceous Piperaceae.Recent studies reported that high leaf conductance is mainly driven by short extraxylary route but was traded off against desiccation resistance.Therefore,we hypothesized that species with a shorter distance between the vein edge and the evaporation site would also have lower desiccation resistance.We computed the farthest diagonal distance from the vein to the lower epidermis from the leaf vein and leaf cross-section images.We then analyzed its correlation with the leaf pressure-volume parameters.Against our expectations,species that had shorter diagonal distances also showed a stronger desiccation resistance.However,the relationship between the diagonal distance and horizontal distance with leaf capacitance was stronger,even stronger than the correlation between leaf capacitance and vein density.This emphasizes the relative importance of leaf capacitance in magnoliid leaves.Our second hypothesis about leaves stated that the leaves of species having strategic vein arrangements would be less expensive to produce.We needed to define a variable that quantifies leaf vein arrangements-the vein arrangement index.Briefly,it quantifies the effect of vein arrangement in shortening the diagonal distance from the vein to the epidermis.As a result,a strategic arrangement of the leaf vein was related to a lower leaf mass per area and freed more surfaces for non-vein tissues.The third hypothesis related to leaf traits stipulates that species with a shorter vein-to-epidermis diagonal length would also have higher theoretical stomatal conductance.The theoretical maximum stomatal conductance was quantified from the stomatal anatomy and density.It was positively correlated with leaf capacitance rather than the diagonal distance(VEd).Basing the stomatal design on capacitance may be a specific strategy for a lineage in a humid habitat.Last but not the least,we combined the data from the stem and leaf structure and function.We aimed to characterize a structured coordination model of the stem and leaf functional traits,a structural model that followed the pathways of water and photosynthate transport.We assumed that the stem-leaf-stem structured network is circular,which means that the correlations between the traits across the network would be significant.The model to be tested was divided into four parts:an upstream(water transport),a downstream(photosynthates translocation),and a radial pathway(the coordination between stem xylem and phloem traits).Along the upstream portion,the correlations between the stem water potential at 50% loss of hydraulic conductivity(P50)and leaf water potential at turgor loss(TLP),between the stem hydraulic conductivity and vein density,and between the stem water storage proxies and leaf capacitance were all weak.Surprisingly,the leaf TLP was more negative than the stem P50.It could be an adaptation to the larger water potential variation in leaves than in stem.Along the downstream portion,we first quantified the fraction of the vascular cross-section area of the midrib and the stem that is occupied by the phloem.Unexpectedly,the correlations between the maximum stomatal conductance and the midrib phloem fraction;and between the midrib phloem fraction and stem phloem fraction were negative,while a positive correlation may have been expected.It was interpreted that the phloem translocation may not have been limiting.The radial portion of the pathway provided evidence of a strong correlation between the axial parenchyma and stem phloem fractions.However,traits coordination along the xylem radial transport pathway was weak,which weakened the continuity of the circular coordination network.In addition,the coordination between the leaf vein and stomata structure was weak.Both the xylem radial transport pathway and leaf extraxylary pathway were functionally significant under dynamic changes in the water status(the capacitance buffers any sudden increase in the vapor pressure deficit;the axial parenchyma protects and repairs the conduits).Instead,trait correlations across xylem water transport and phloem photosynthate translocation were always significant.In conclusion,the xylem parenchyma arrangement and leaf vein placement are low-cost alternatives that may help the entire organism to operate at the best of its capacity.The integration of both the tissue fraction and spatial arrangement can provide important knowledge on the functional significance of plant anatomy.Our study stands as a pioneer in the quantification of tissue spatial arrangement and its contribution to the functional efficiency of the organism.Therefore,we call for a standardized method that quantifies tissue spatial arrangement and its functional significance.