The ultrastructure of chilling stress

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Abstract
Chilling injury to crop plants was first described 70 years ago and has been systematically investigated with electron microscopy since the late 1960s. Chloroplasts are the first and most severely impacted organelle. Thylakoids swell and distort, starch granules disappear, and a peripheral reticulum (vesicles arising from inner membrane of chloroplast envelope) appears. Chloroplast disintegration follows prolonged chilling. Mitochondria, nuclei and other organelles are less susceptible to chilling injury. Organellar development and ontogeny may also be disrupted. The inherent chilling sensitivity of a plant, as well as the ability of some species to acclimate to chilling, influence the timing and appearance of ultrastructural injury with the resulting outcome being mild, moderate, or severe. Other environmental factors that exacerbate injury are irradiance, chilling duration, and water status. The physiological basis for chloroplast swelling may be linked to chilling‐stable starch‐degrading enzymes that produce soluble sugars thus lowering stromal water potential at a time when chloroplast photosynthate export is reduced. Thylakoid dilation appears to be related to photo‐oxidative conditions produced during chilling in the light. The peripheral reticulum is proposed to increase surface area of the transport‐limiting membrane (chloroplast inner membrane) in response to the chilling‐induced reduction in metabolite transport. Many of the ultrastructural symptoms appearing during moderate stress resemble those seen in programmed cell death. Future research directions are discussed.