Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation‐induced flooding of the mesophyll

Abstract

Why the leaves of cold temperate deciduous and moistureloving angiosperms are so often toothed has long puzzled biologists because the functional consequences of teeth remain poorly understood. Here we provide functional and structural evidence that marginal leaf teeth of Chloranthus japonicus , an understory herb, enable the release of guttation sap during root pressure. When guttation from teeth hydathodes was experimentally blocked, we found that the leaf intercellular airspaces became flooded. Measurements of chlorophyll a fluorescence revealed that internal flooding resulted in an inhibition of photosynthesis, most likely through the formation of a film of water within the leaf that reduced CO 2 diffusion. Comparing a developmental series of leaves with and without teeth experimentally covered with wax, we found that teeth did not affect overall leaf stomatal conductance and CO 2 uptake. However, maximal and effective light-saturation PSII quantum yields of teeth were found to be lower or equal to the surrounding lamina throughout leaf ontogeny. Collectively, our results suggest hydathodes and their development on teeth apices enable the avoidance of mesophyll flooding by root pressure. We discuss how these new findings bear on the potential physiological interpretations of models that apply leaf marginal traits to infer ancient climates.

Causes of ecological gradients in leaf margin entirety: Evaluating the roles of biomechanics, hydraulics, vein geometry, and bud packing

“…Th is function would allow plants to refi ll xylem embolisms or drive leaf expansion without reducing photosynthesis via greatly increased resistance to CO 2 diff usion through water vs. air. Th eir experiments on Chloranthus japonicus support this conclusion; the mesophyll of leaves with intact hydathodes did not fl ood, while those with blocked hydathodes lost up to 40% of PSII photon yields, potentially for hours in highly humid habitats ( Feild et al, 2005 ). Hydathodal teeth may thus be adaptive for cold temperate plants seeking to refi ll freeze-thaw embolisms ( Edwards et al, 2016 ).…”

“…Th in leaves should also select for thicker veins with more mechanical tissue to support the otherwise fl oppy lamina. In many species, high fl ow rates in thin leaves may also lead to greater risks of embolism within the leaf, selecting for root pressure to heal embolisms, especially in larger veins ( Brodribb et al, 2016 ), selecting in another way for craspedodromous or semicraspedodromous venation leading to the leaf margin and hydathodal teeth to prevent fl ooding of the mesophyll and possibly loss of photosynthetic capacity ( Feild et al, 2005 ) ( Fig. 6 ).…”

“…(4) Hydathodal teeth -Following earlier suggestions ( Haberlandt, 1914 ;Rea, 1929 ), Feild et al (2005) proposed that hydathodal teeth prevent water supplied by root pressure from fl ooding the mesophyll. Th is function would allow plants to refi ll xylem embolisms or drive leaf expansion without reducing photosynthesis via greatly increased resistance to CO 2 diff usion through water vs. air.…”

“…Th e frequent placement of hydathodes on marginal teeth may also allow the leaves to shed exudate rapidly and avoid damage by pathogens or epiphylls, with the teeth acting as minidrip tips ( Feild et al, 2005 ).…”

Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous

“…Teeth of this type are sites of guttation; the loss of water at tooth apices prevents flooding of the leaf mesophyll under conditions of high soil moisture, high humidity and low evaporative demand [53][54][55]. Environments such as forest understory and riparian corridors in tropical and temperate climates typically host plants with hydathodal teeth [49,[56][57][58][59][60][61]; but hydathodal teeth also occur in some marginally or semi-aquatic ranunculalean herbs that grow under bright, subareal conditions [39].…”