A purple acid phosphatase, GmPAP33, participates in arbuscule degeneration during arbuscular mycorrhizal symbiosis in soybean

Abstract

Arbuscules are the central structures of the symbiotic association between terrestrial plants and arbuscular mycorrhizal (AM) fungi. However, arbuscules are also ephemeral structures, and following development, these structures are soon digested and ultimately disappear. Currently, little is known regarding the mechanism underlying the digestion of senescent arbuscules. Here, biochemical and functional analyses were integrated to test the hypothesis that a purple acid phosphatase, GmPAP33, controls the hydrolysis of phospholipids during arbuscule degeneration. The expression of GmPAP33 was enhanced by AM fungal inoculation independent of the P conditions in soybean roots. Promoter‐β‐glucuronidase (GUS) reporter assays revealed that the expression of GmPAP33 was mainly localized to arbuscule‐containing cells during symbiosis. The recombinant GmPAP33 exhibited high hydrolytic activity towards phospholipids, phosphatidylcholine, and phosphatidic acid. Furthermore, soybean plants overexpressing GmPAP33 exhibited increased percentages of large arbuscules and improved yield and P content compared with wild‐type plants when inoculated with AM fungi. Mycorrhizal RNAi plants had high phospholipid levels and a large percentage of small arbuscules. These results in combination with the subcellular localization of GmPAP33 at the plasma membrane indicate that GmPAP33 participates in arbuscule degeneration during AM symbiosis via involvement in phospholipid hydrolysis.

Linking lipid transfer with reduced arbuscule formation in tomato roots colonized by arbuscular mycorrhizal fungus under low pH stress

“…SlPAP20, which is homologous to GmPAP33 (Li et al ., ), may be involved in PLFA hydrolysis. We found that AM fungal inoculation significantly increased SlPAP20 expression at pH 6.5 but did not affect it at pH 4.5 (Fig.…”

“…Recently, Li et al . () demonstrated that a purple acid phosphatase (GmPAP33) participated in arbuscule degeneration via involvement in phospholipid hydrolysis in soybean; therefore, we additionally investigated the relative expression of a homologous gene ( SlPAP20 ). The sequences of the primers for all genes are described in Table S1, and the unpublished primers without known references, including those for genes RAM2 , STR , STR2 , SISUT1 , 2 , 4 , SISTP1 , LIN6 and SIPAP20 , were designed with Primer Premier Version 5.00 (http://www.premierbiosoft.com) in this study.…”

“…In yeast, however, phospholipase B of fungal origin is the key player in phospholipid hydrolysis (Ferreira et al, 2018). More recently, Li et al (2019) proposed that a purple acid phosphatase of soybean origin participated in the hydrolysis of phospholipids in arbuscule membranes during arbuscule degeneration. It is possible that hydrolytic enzymes of plant origin play main roles in hydrolysing fungal phospholipids in plant-fungal symbionts, which requires finetuned but yet unknown molecular communication between two partners.…”

“…To investigate the effect of pH on AM fungal functioning (P nutrition), lipid and sugar transfer between symbionts, we analysed the expression of 17 genes involved in P transport (SlPT1~5, SlHA8), lipid biosynthesis (RAM2) and transport (STR, STR2), sugar transport (SlSWEET2b, SlSWEET14, SlSUT1, SlSUT2, SlSUT4, SlST3, SlSTP1, LIN6). Recently, Li et al (2019) demonstrated that a purple acid phosphatase (GmPAP33) participated in arbuscule degeneration via involvement in phospholipid hydrolysis in soybean; therefore, we additionally investigated the relative expression of a homologous gene (SlPAP20). The sequences of the primers for all genes are described in Table S1, and the unpublished primers without known references, including those for genes RAM2, STR, STR2, SISUT1,2,4, SISTP1, LIN6 and SIPAP20, were designed with Primer Premier Version 5.00 (www.PremierBiosoft.…”

The Infection Unit: An Overlooked Conceptual Unit for Arbuscular Mycorrhizal Function

“…Recently, several mutant lines exhibited suppressed intraradical colonization, forming prematurely senescent or stunted arbuscules [11,31]. Some plant genes have been implicated in the cellular process of arbuscule degeneration [32][33][34][35]. The degeneration process of arbuscules has also been shown to be related to colonization level, illustrating the importance of arbuscule life cycle to the development of mycorrhiza.…”