Phospholipase Dα1-mediated phosphatidic acid change is a key determinant of desiccation-induced viability loss in seeds.
High sensitivity of seeds to water loss is a widespread phenomenon in the world's plant species. The molecular basis of this trait is poorly understood but thought to be associated with critical changes in membrane function. We profiled membrane lipids of seeds in eight species with varying levels of desiccation tolerance and found a close association between reducing seed viability and increasing phosphatidic acid (PA). We applied hydration-dehydration cycles to Arabidopsis seeds, which are normally desiccation tolerant, to mimic the onset of desiccation sensitivity with progression towards germination and examined the role of phospholipase D (PLD) in desiccation stress-induced production of PA. We found that PLDα1 became more abundant and migrated from the cytosol to the membrane during desiccation, whereas PLDδ did not change, and that all desiccation-induced PA was derived from PLDα1 hydrolysis. When PLDα1 was suppressed, the germination level after each hydration-dehydration cycle improved significantly. We further demonstrated that PLDα1-mediated PA formation modulates desiccation sensitivity as applying its inhibitor improved seed desiccation tolerance and its suppression in protoplasts enhanced survival under dehydration. The insights provided by comparative lipidomics enable us to propose a new membrane-based model for seed desiccation stress and survival.
Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.|Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.
Hongying
H
Chen
Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.
Xiaomei
X
Yu
Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.
Xudong
X
Zhang
Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.
Lan
L
Yang
Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.|Department of Phytopathology, College of Plant Protection, Yunnan Agriculture University, 650201, China.
Xing
X
Huang
Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.
Jie
J
Zhang
Royal Botanic Gardens, Kew, Wakehurst Place, West Sussex, RH17 6TN, UK.
Hugh W
HW
Pritchard
Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.|Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.
Weiqi
http://orcid.org/0000-0003-4988-4516
W
Li
D000222:Adaptation, Physiological / Q000187:drug effects; D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D002462:Cell Membrane / Q000187:drug effects / Q000378:metabolism; D018548:Cotyledon / Q000378:metabolism; D003593:Cytoplasm / Q000187:drug effects / Q000378:metabolism; D003890:Desiccation; D004791:Enzyme Inhibitors / Q000494:pharmacology; D018525:Germination / Q000187:drug effects; D008055:Lipids / Q000032:analysis; D010712:Phosphatidic Acids / Q000378:metabolism*; D010739:Phospholipase D / Q000378:metabolism*; D021381:Protein Transport / Q000187:drug effects; D011523:Protoplasts / Q000187:drug effects / Q000378:metabolism; D012639:Seeds / Q000187:drug effects / Q000201:enzymology* / Q000502:physiology*; D013045:Species Specificity; D013347:Subcellular Fractions / Q000187:drug effects / Q000378:metabolism; D014022:Tissue Survival / Q000187:drug effects / Q000502:physiology*
D029681:Arabidopsis Proteins; D004791:Enzyme Inhibitors; D008055:Lipids; D010712:Phosphatidic Acids; C582894:PLDA1 protein, Arabidopsis; D010739:Phospholipase D
drought; membrane lipid; phosphatidic acid (PA); phospholipase D (PLD); seed storage behaviour; water relation