TY - JOUR

T1 - Hypoxia in tomato (Solanum lycopersicum) fruit during ripening

T2 - Biophysical elucidation by a 3D reaction–diffusion model

AU - Xiao, Hui

AU - Verboven, Pieter

AU - Tong, Shuai

AU - Pedersen, Ole

AU - Nicolaï, Bart

PY - 2024

Y1 - 2024

N2 - Respiration provides energy, substrates, and precursors to support physiological changes of the fruit during climacteric ripening. A key substrate of respiration is oxygen that needs to be supplied to the fruit in a passive way by gas transfer from the environment. Oxygen gradients may develop within the fruit due to its bulky size and the dense fruit tissues, potentially creating hypoxia that may have a role in the spatial development of ripening. This study presents a 3D reaction–diffusion model using tomato (Solanum lycopersicum) fruit as a test subject, combining the multiscale fruit geometry generated from magnetic resonance imaging and microcomputed tomography with varying respiration kinetics and contrasting boundary resistances obtained through independent experiments. The model predicted low oxygen levels in locular tissue under atmospheric conditions, and the oxygen level was markedly lower upon scar occlusion, aligning with microsensor profiling results. The locular region was in a hypoxic state, leading to its low aerobic respiration with high CO2 accumulation by fermentative respiration, while the rest of the tissues remained well oxygenated. The model further revealed that the hypoxia is caused by a combination of diffusion resistances and respiration rates of the tissue. Collectively, this study reveals the existence of the respiratory gas gradients and its biophysical causes during tomato fruit ripening, providing richer information for future studies on localized endogenous ethylene biosynthesis and fruit ripening.

AB - Respiration provides energy, substrates, and precursors to support physiological changes of the fruit during climacteric ripening. A key substrate of respiration is oxygen that needs to be supplied to the fruit in a passive way by gas transfer from the environment. Oxygen gradients may develop within the fruit due to its bulky size and the dense fruit tissues, potentially creating hypoxia that may have a role in the spatial development of ripening. This study presents a 3D reaction–diffusion model using tomato (Solanum lycopersicum) fruit as a test subject, combining the multiscale fruit geometry generated from magnetic resonance imaging and microcomputed tomography with varying respiration kinetics and contrasting boundary resistances obtained through independent experiments. The model predicted low oxygen levels in locular tissue under atmospheric conditions, and the oxygen level was markedly lower upon scar occlusion, aligning with microsensor profiling results. The locular region was in a hypoxic state, leading to its low aerobic respiration with high CO2 accumulation by fermentative respiration, while the rest of the tissues remained well oxygenated. The model further revealed that the hypoxia is caused by a combination of diffusion resistances and respiration rates of the tissue. Collectively, this study reveals the existence of the respiratory gas gradients and its biophysical causes during tomato fruit ripening, providing richer information for future studies on localized endogenous ethylene biosynthesis and fruit ripening.

U2 - 10.1093/plphys/kiae174

DO - 10.1093/plphys/kiae174

M3 - Journal article

C2 - 38546393

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

ER -