Mechanical Failure of Fine Root Cortical Cells Initiates Plant Hydraulic Decline during Drought

Abstract

Root systems perform the crucial task of absorbing water from the soil to meet the demands of a transpiring canopy. Roots are thought to operate like electrical fuses, which break when carrying an excessive load under conditions of drought stress. Yet the exact site and sequence of this dysfunction in roots remain elusive. Using in vivo x-ray computed microtomography, we found that drought-induced mechanical failure (i.e. lacunae formation) in fine root cortical cells is the initial and primary driver of reduced fine root hydraulic conductivity (Lp r ) under mild to moderate drought stress. Cortical lacunae started forming under mild drought stress (20.6 MPa C stem ), coincided with a dramatic reduction in Lp r , and preceded root shrinkage or significant xylem embolism. Only under increased drought stress was embolism formation observed in the root xylem, and it appeared first in the fine roots (50% loss of hydraulic conductivity [P 50 ] reached at 21.8 MPa) and then in older, coarse roots (P 50 = 23.5 MPa). These results suggest that cortical cells in fine roots function like hydraulic fuses that decouple plants from drying soil, thus preserving the hydraulic integrity of the plant's vascular system under early stages of drought stress. Cortical lacunae formation led to permanent structural damage of the root cortex and nonrecoverable Lp r , pointing to a role in fine root mortality and turnover under drought stress.

Stomatal Closure, Basal Leaf Embolism, and Shedding Protect the Hydraulic Integrity of Grape Stems

“…According to the segmentation hypothesis, plants sacrifice organs of lesser importance and investment to save organs that are critical for longterm survival and propagation (Zimmermann, 1983). Such segmentation is supported in grapevine by the finding that petioles and roots are more vulnerable to cavitation than stems (Lovisolo et al, 2008;Charrier et al, 2016;Cuneo et al, 2016;Hochberg et al, 2016a). Combining these previous findings with our observation that, on average, the midrib cavitates before higher vein orders (for clear visualization, see Supplemental Fig.…”

Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland

“…Our finding is consistent with recent studies on potted individuals showing an association between the onset of optically observed xylem embolism and loss of hydraulic function in leaves across several plant functional types (Brodribb et al ., ; Hochberg et al ., ; Skelton et al ., ). Although hydraulic impairment at low leaf water potential has consistently been shown to be caused by embolism (Brodribb et al ., ; Hochberg et al ., ; Skelton et al ., ), other mechanisms may also reduce k leaf (Cuneo et al ., ; Scoffoni et al ., ).…”

Co‐occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought

“…However, rather than experience this PLC in the branches or roots, the large loss of conductivity in this study appeared to occur below ground in locations or tissues other than coarse roots. Possible explanations for how this belowground hydraulic conductance would decline in situ are either declines in soil hydraulic conductivity, mechanical failure (i.e., roots no longer in contact with soil particles), hydraulic failure of fine root cortical cells or fine root embolism upon exposure to drying soil (Cuneo, Knipfer, Brodersen, & McElrone, ).…”