TY - JOUR
T1 - Alternate modes of photosynthate transport in the alternating generations of physcomitrella patens
AU - Regmi, Kamesh C.
AU - Li, Lin
AU - Gaxiola, Roberto
N1 - Funding Information:
This work was supported by the National Science Foundation [grant number: IOS-1122148 to KR and RG], and International Wheat Yield Partnership [IWYP to KR, LL, and RG].
Publisher Copyright:
© 2017 Regmi, Li and Gaxiola.
PY - 2017/11/13
Y1 - 2017/11/13
N2 - Physcomitrella patens has emerged as a model moss system to investigate the evolution of various plant characters in early land plant lineages. Yet, there is merely a disparate body of ultrastructural and physiological evidence from other mosses to draw inferences about the modes of photosynthate transport in the alternating generations of Physcomitrella. We performed a series of ultrastructural, fluorescent tracing, physiological, and immunohistochemical experiments to elucidate a coherent model of photosynthate transport in this moss. Our ultrastructural observations revealed that Physcomitrella is an endohydric moss with water-conducting and putative food-conducting cells in the gametophytic stem and leaves. Movement of fluorescent tracer 5(6)-carboxyfluorescein diacetate revealed that the mode of transport in the gametophytic generation is symplasmic and is mediated by plasmodesmata, while there is a diffusion barrier composed of transfer cells that separates the photoautotrophic gametophyte from the nutritionally dependent heterotrophic sporophyte. We posited that, analogous to what is found in apoplasmically phloem loading higher plants, the primary photosynthate sucrose, is actively imported into the transfer cells by sucrose/H+ symporters (SUTs) that are, in turn, powered by P-type ATPases, and that the transfer cells harbor an ATP-conserving Sucrose Synthase (SUS) pathway. Supporting our hypothesis was the finding that a protonophore (2,4-dinitrophenol) and a SUT-specific inhibitor (diethyl pyrocarbonate) reduced the uptake of radiolabeled sucrose into the sporangia. In situ immunolocalization of P-type ATPase, Sucrose Synthase, and Proton Pyrophosphatase – all key components of the SUS pathway – showed that these proteins were prominently localized in the transfer cells, providing further evidence consistent with our argument.
AB - Physcomitrella patens has emerged as a model moss system to investigate the evolution of various plant characters in early land plant lineages. Yet, there is merely a disparate body of ultrastructural and physiological evidence from other mosses to draw inferences about the modes of photosynthate transport in the alternating generations of Physcomitrella. We performed a series of ultrastructural, fluorescent tracing, physiological, and immunohistochemical experiments to elucidate a coherent model of photosynthate transport in this moss. Our ultrastructural observations revealed that Physcomitrella is an endohydric moss with water-conducting and putative food-conducting cells in the gametophytic stem and leaves. Movement of fluorescent tracer 5(6)-carboxyfluorescein diacetate revealed that the mode of transport in the gametophytic generation is symplasmic and is mediated by plasmodesmata, while there is a diffusion barrier composed of transfer cells that separates the photoautotrophic gametophyte from the nutritionally dependent heterotrophic sporophyte. We posited that, analogous to what is found in apoplasmically phloem loading higher plants, the primary photosynthate sucrose, is actively imported into the transfer cells by sucrose/H+ symporters (SUTs) that are, in turn, powered by P-type ATPases, and that the transfer cells harbor an ATP-conserving Sucrose Synthase (SUS) pathway. Supporting our hypothesis was the finding that a protonophore (2,4-dinitrophenol) and a SUT-specific inhibitor (diethyl pyrocarbonate) reduced the uptake of radiolabeled sucrose into the sporangia. In situ immunolocalization of P-type ATPase, Sucrose Synthase, and Proton Pyrophosphatase – all key components of the SUS pathway – showed that these proteins were prominently localized in the transfer cells, providing further evidence consistent with our argument.
KW - Apoplasmic transport
KW - P-type H ATPase
KW - Physcomitrella patens
KW - Proton pyrophosphatase
KW - Sucrose synthase pathway
KW - Sucrose/H symporter
KW - Symplasmic transport
KW - Transfer cells
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UR - http://www.scopus.com/inward/citedby.url?scp=85034057979&partnerID=8YFLogxK
U2 - 10.3389/fpls.2017.01956
DO - 10.3389/fpls.2017.01956
M3 - Article
AN - SCOPUS:85034057979
SN - 1664-462X
VL - 8
JO - Frontiers in Plant Science
JF - Frontiers in Plant Science
M1 - 1956
ER -