A secretory phospholipase D hydrolyzes phosphatidylcholine to suppress rice heading time

Abstract

Phospholipase D (PLD) hydrolyzes membrane phospholipids and is crucial in various physiological processes and transduction of different signals. Secretory phospholipases play important roles in mammals, however, whose functions in plants remain largely unknown. We previously identified a rice secretory PLD (spPLD) that harbors a signal peptide and here we reported the secretion and function of spPLD in rice heading time regulation. Subcellular localization analysis confirmed the signal peptide is indispensable for spPLD secretion into the extracellular spaces, where spPLD hydrolyzes substrates. spPLD overexpression results in delayed heading time which is dependent on its secretory character, while suppression or deficiency of spPLD led to the early heading of rice under both short-day and long-day conditions, which is consistent with that spPLD overexpression/suppression indeed led to the reduced/increased Hd3a/RFT1 (Arabidopsis Flowing Locus T homolog) activities. Interestingly, rice Hd3a and RFT1 bind to phosphatidylcholines (PCs) and a further analysis by lipidomic approach using mass spectrometry revealed the altered phospholipids profiles in shoot apical meristem, particularly the PC species, under altered spPLD expressions. These results indicate the significance of secretory spPLD and help to elucidate the regulatory network of rice heading time.

An adaptive teosintemexicanaintrogression modulates phosphatidylcholine levels and is associated with maize flowering time

“…ZCN8 is a close ortholog of Arabidopsis FT , whose encoding protein interacts with several species of phospholipids to modulate flowering time (43; 41). A similar interaction was also demonstrated for the rice FT ortholog Hd3a, (76) and we hypothesize that the same may be occurring in maize. Comparison of docking simulations of phospholipids with ZCN8 using the Arabidopsis FT crystal structures as a model (70) showed similar PC interactions in ZCN8 (Fig.…”

“…Similarly, PG species can sequester FT in phloem companion cells in low temperatures (41) and then release FT into the phloem later after temperatures increase, allowing FT reach the shoot apical meristem. In agreement with an effect of lipids on flowering time, overexpression of a gene encoding a secretory phospholipase D delayed heading time in rice (76). In line with a role for phospholipids in flowering, we established that genetic variation at SNPs within the region of HPC1 encoding the lipase domain exhibits a strong interaction with elevation for the highland HPC1-PT allele.…”

“…Phospholipids are key structural components of plant membranes that also function as signaling molecules during adaptation to stresses that would be prevalent in highland environments (58; 71) such as low phosphorus availability (72; 73; 74) and low temperatures (35; 36; 75). In Arabidopsis and rice ( Oryza sativa , phospholipid species regulate flowering time via interactions with Arabidopsis FT and rice Heading date 3a (Hd3a), respectively (43; 41; 76). Flowering time is a major driver of maize adaptation to highland environments (19; 20; 77) and to northern latitudes (27; 26).…”

An adaptive teosintemexicanaintrogression modulates phosphatidylcholine levels and is associated with maize flowering time

“…Phospholipids are key structural components of plant membranes that also function as signaling molecules during adaptation to stresses that would be prevalent in highland environments ( 52 , 67 ) such as low phosphorus availability ( 68 – 70 ) and low temperatures ( 30 , 31 , 71 ). In Arabidopsis and rice ( Oryza sativa ), phospholipid species regulate flowering time via interactions with Arabidopsis FT and rice Heading date 3a (Hd3a), respectively ( 36 , 38 , 72 ). Flowering time is a major driver of maize adaptation to highland environments ( 15 , 44 , 73 ) and to northern latitudes ( 21 , 22 ).…”

Characterization and evolutionary diversification of the phospholipase D gene family in mosses

“…In addition to C2 and PX/ PH PLDs, there is another type of phospholipase referred to as signal peptide (SP) PLD, which lacks the C2 and PX/PH domains but carrying an N-terminal signal peptide (Selvy et al, 2011). With the help of a signal peptide, SP PLD is secreted into the extracellular spaces to hydrolyze its substrates (Qu et al, 2021). In rice, SP PLD expression was downregulated during the entire reproductive stage (Singh et al, 2012).…”