How megadrought causes extensive mortality in a deep-rooted shrub species normally resistant to drought-induced dieback: The role of a biotic mortality agent.

Southern California experienced unprecedented megadrought between 2012 and 2018. During this time, Malosma laurina, a chaparral species normally resilient to single-year intense drought, developed extensive mortality exceeding 60% throughout low-elevation coastal populations of the Santa Monica Mountains. We assessed the physiological mechanisms by which the advent of megadrought predisposed M. laurina to extensive shoot dieback and whole-plant death. We found that hydraulic conductance of stem xylem (Ks, native ) was reduced seven to 11-fold in dieback adult and resprout branches, respectively. Staining of stem xylem vessels revealed that dieback plants experienced 68% solid-blockage, explaining the reduction in water transport. Following Koch's postulates, persistent isolation of a microorganism in stem xylem of dieback plants but not healthy controls indicated that the causative agent of xylem blockage was an opportunistic endophytic fungus, Botryosphaeria dothidea. We inoculated healthy M. laurina saplings with fungal isolates and compared hyphal elongation rates under well-watered, water-deficit, and carbon-deficit treatments. Relative to controls, we found that both water deficit and carbon-deficit increased hyphal extension rates and the incidence of shoot dieback.

Polyploid goldback and silverback ferns (Pentagramma) occupy a wider, colder, and wetter bioclimatic niche than diploid counterparts.

PREMISE: The western North American fern genus Pentagramma (Pteridaceae) is characterized by complex patterns of ploidy variation, an understanding of which is critical to comprehending both the evolutionary processes within the genus and its current diversity. METHODS: We undertook a cytogeographic study across the range of the genus, using a combination of chromosome counts and flow cytometry to infer ploidy level. Bioclimatic variables and elevation were used to compare niches. RESULTS: We found that diploids and tetraploids are common and widespread, and triploids are rare and sporadic; in contrast with genome size inferences in earlier studies, no hexaploids were found. Diploids and tetraploids show different geographic ranges: only tetraploids were found in the northernmost portion of the range (Washington, Oregon, and British Columbia) and only diploids were found in the Sierra Nevada of California. Diploid, triploid, and tetraploid cytotypes were found to co-occur in relatively few localities: in the southern (San Diego County, California) and desert Southwest (Arizona) parts of the range, and along the Pacific Coast of California. CONCLUSIONS: Tetraploids occupy a wider bioclimatic niche than diploids both within P. triangularis and at the genus-wide scale. It is unknown whether the wider niche of tetraploids is due to their expansion upon the diploid niche, if diploids have contracted their niche due to competition or changing abiotic conditions, or if this wider niche occupancy is due to multiple origins of tetraploids.

A reduced role for water transport during the Cenozoic evolution of epiphytic Eupolypod ferns.

The Cretaceous-Cenozoic expansion of tropical forests created canopy space that was subsequently occupied by diverse epiphytic communities including Eupolypod ferns. Eupolypods proliferated in this more stressful niche, where lower competition enabled the adaptive radiation of thousands of species. Here, we examine whether xylem traits helped shape the Cenozoic radiation of Eupolypod ferns. We characterized the petiole xylem anatomy of 39 species belonging to the Eupolypod I and Eupolypod II clades occupying the epiphytic, hemiepiphytic, and terrestrial niche, and we assessed vulnerability to embolism in a subset of species. The transition to the canopy was associated with reduced xylem content and smaller tracheid diameters, but no differences were found in species vulnerability to embolism and pit membrane thickness. Phylogenetic analyses support selection for traits associated with reduced water transport in Eupolypod 1 species. We posit that in Eupolypod epiphytes, selection favored water retention via thicker leaves and lower stomatal density over higher rates of water transport. Consequently, lower leaf water loss was coupled with smaller quantities of xylem and narrower tracheid diameters. Traits associated with water conservation were evident in terrestrial Eupolypod 1 ferns and may have predisposed this clade toward radiation in the canopy.

Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms.

Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi-epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi-epiphytic and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (-63%), shorter stipe lengths (-56%), thicker laminae (+41%) and reduced stomatal density (-46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi-epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi-epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely evolutionarily constrained physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat.

Foliar water uptake via cork warts in mangroves of the Sonneratia genus.

Foliar water uptake (FWU) occurs in plants of diverse ecosystems; however, the diversity of pathways and their associated FWU kinetics remain poorly resolved. We characterized a novel FWU pathway in two mangrove species of the Sonneratia genus, S. alba and S. caseolaris. Further, we assessed the influence of leaf wetting duration, wet-dry seasonality and leaf dehydration on leaf conductance to surface water (Ksurf ). The symplastic tracer dye, disodium fluorescein, revealed living cells subtending and encircling leaf epidermal structures known as cork warts as a pathway of FWU entry into the leaf. Rehydration kinetics experiments revealed a novel mode of FWU, with slow and steady rates of water uptake persistent over a duration of 12 hr. Ksurf increased with longer durations of leaf wetting and was greater in leaves with more negative water potentials at the initiation of leaf wetting. Ksurf declined by 68% between wet and dry seasons. Our results suggest that FWU via cork warts in Sonneratia sp. may be rate limited and under active regulation. We conclude that FWU pathways in halophytes may require ion exclusion to avoid uptake of salt when inundated, paralleling the capacity of halophyte roots for ion selectivity during water acquisition.

Positive root pressure is critical for whole-plant desiccation recovery in two species of terrestrial resurrection ferns.

Desiccation-tolerant (DT) organisms can lose nearly all their water without dying. Desiccation tolerance allows organisms to survive in a nearly completely dehydrated, dormant state. At the cellular level, sugars and proteins stabilize cellular components and protect them from oxidative damage. However, there are few studies of the dynamics and drivers of whole-plant recovery in vascular DT plants. In vascular DT plants, whole-plant desiccation recovery (resurrection) depends not only on cellular rehydration, but also on the recovery of organs with unequal access to water. In this study, in situ natural and artificial irrigation experiments revealed the dynamics of desiccation recovery in two DT fern species. Organ-specific irrigation experiments revealed that the entire plant resurrected when water was supplied to roots, but leaf hydration alone (foliar water uptake) was insufficient to rehydrate the stele and roots. In both species, pressure applied to petioles of excised desiccated fronds resurrected distal leaf tissue, while capillarity alone was insufficient to resurrect distal pinnules. Upon rehydration, sucrose levels in the rhizome and stele dropped dramatically as starch levels rose, consistent with the role of accumulated sucrose as a desiccation protectant. These findings provide insight into traits that facilitate desiccation recovery in dryland ferns associated with chaparral vegetation of southern California.

High-resolution computed tomography reveals dynamics of desiccation and rehydration in fern petioles of a desiccation-tolerant fern.

Desiccation-tolerant (DT) plants can dry past -100 MPa and subsequently recover function upon rehydration. Vascular DT plants face the unique challenges of desiccating and rehydrating complex tissues without causing structural damage. However, these dynamics have not been studied in intact DT plants. We used high resolution micro-computed tomography (microCT), light microscopy, and fluorescence microscopy to characterize the dynamics of tissue desiccation and rehydration in petioles (stipes) of intact DT ferns. During desiccation, xylem conduits in stipes embolized before cellular dehydration of living tissues within the vascular cylinder. During resurrection, the chlorenchyma and phloem within the stipe vascular cylinder rehydrated before xylem refilling. We identified unique stipe traits that may facilitate desiccation and resurrection of the vascular system, including xylem conduits containing pectin (which may confer flexibility and wettability); chloroplasts within the vascular cylinder; and an endodermal layer impregnated with hydrophobic substances that impede apoplastic leakage while facilitating the upward flow of water within the vascular cylinder. Resurrection ferns are a novel system for studying extreme dehydration recovery and embolism repair in the petioles of intact plants. The unique anatomical traits identified here may contribute to the spatial and temporal dynamics of water movement observed during desiccation and resurrection.

Seasonal changes in tissue-water relations for eight species of ferns during historic drought in California.

PREMISE OF THE STUDY: California experienced severe drought between 2012 and 2016. During this period, we compared seasonal changes in tissue-water relations among eight fern species in the Santa Monica Mountains of southern California to elucidate differential mechanisms of drought survival and physiological performance during extreme water deficits. METHODS: We monitored seasonal changes in water potential (Ψmd) and dark-adapted chlorophyll fluorescence (Fv/Fm), assessed tissue-water relations including osmotic potential at saturation and the turgor loss point (Ψπ, sat and Ψπ, tlp), and measured, for two evergreen species, xylem-specific and leaf-specific hydraulic conductivity (Ks and Kl) and vulnerability of stem xylem to water stress-induced embolism (water potential at 50% loss hydraulic conductivity, Ψ50). KEY RESULTS: Species grew in either riparian or chaparral understory. The five chaparral species had a wider range of seasonal water potentials, root depths, and frond phenological traits, including one evergreen, two summer-deciduous, and two desiccation-tolerant (resurrection) species. Evergreen species were especially diverse, with an evergreen riparian species maintaining seasonal water potentials above -1.3 MPa, while an evergreen chaparral species had seasonal water potentials below -8 MPa. In those two species the Ψ50 values were -2.5 MPa and -4.3 MPa, respectively. CONCLUSIONS: Observed differences in physiological performance among eight fern species reflected niche partitioning in water utilization and habitat preference associated with distinct phenological traits. We predict differential survival among fern species as future drought events in California intensify, with desiccation-tolerant resurrection ferns being the most resistant.