The Plastid Envelope CHLOROPLAST MANGANESE TRANSPORTER1 Is Essential for Manganese Homeostasis in Arabidopsis

Abstract

The transition metal manganese (Mn) is indispensable for photoautotrophic growth since photosystem II (PSII) employs an inorganic MnCaO cluster for water splitting. Here, we show that the Arabidopsis membrane protein CHLOROPLAST MANGANESE TRANSPORTER1 (CMT1) is involved in chloroplast Mn homeostasis. CMT1 is the closest homolog of the previously characterized thylakoid Mn transporter PHOTOSYNTHESIS-AFFECTED MUTANT71 (PAM71). In contrast to PAM71, CMT1 resides at the chloroplast envelope and is ubiquitously expressed. Nonetheless, like PAM71, the expression of CMT1 can also alleviate the Mn-sensitive phenotype of yeast mutant Δpmr1. The cmt1 mutant is severely suppressed in growth, chloroplast ultrastructure, and PSII activity owing to a decrease in the amounts of pigments and thylakoid membrane proteins. The importance of CMT1 for chloroplast Mn homeostasis is demonstrated by the significant reduction in chloroplast Mn concentrations in cmt1-1, which exhibited reduced Mn binding in PSII complexes. Moreover, CMT1 expression is downregulated in Mn-surplus conditions. The pam71 cmt1-1double mutant resembles the cmt1-1 single mutant rather than pam71 in most respects. Taken together, our results suggest that CMT1 mediates Mn uptake into the chloroplast stroma, and that CMT1 and PAM71 function sequentially in Mn delivery to PSII across the chloroplast envelope and the thylakoid membrane.

Manganese in Plants: From Acquisition to Subcellular Allocation

“…Like AtBICAT1, the expression of AtBICAT2 can also alleviate the Mn 2+ and Ca 2+ sensitivity phenotypes of the pmr1 and pmr1gdt1 yeast mutants, respectively. Disruption of AtBICAT2 resulted in strong chlorosis, severely impaired plant growth, defective thylakoid stacking, and severe reduction of PS II complexes, resulting in diminished photosynthetic activity (Eisenhut et al, 2018;Frank et al, 2019). Consistent with a reduced oxygen evolution capacity, bicat2 mutant chloroplasts contained less Mn than those of the wild type (Zhang et al, 2018).…”

“…AtBICAT2 (syn. PAM71HL, CMT1), the second member of this family, was also described to fulfill functions in chloroplast Mn and Ca 2+ homeostasis (Eisenhut et al, 2018;Frank et al, 2019). In contrast to AtBICAT1, it resides in the chloroplast envelope.…”

Chloroplast Calcium Signaling in the Spotlight

“…Altogether, these channels/ transporters can be involved in the formation of the plastidial Ca 2+ transients, along with the putative calcium-transporting protein PAM71/BICAT (Frank et al, 2019). However, this latter protein seems to play a prevalent role in manganese homeostasis rather than in calcium homeostasis (Schneider et al, 2016; Dammann et al, 2003;Nühse et al, 2003;Nühse et al, 2004;Benschop et al, 2007;Chen et al, 2010;Keinath et al, 2010;Zhang and Peck, 2011;Elmore et al, 2012;Zargar et al, 2015;Zou et al, 2015 At5g24430 AtCRK4 Calcium Dunkley et al, 2006;Benschop et al, 2007;Anil et al, 2008;Zhang and Peck, 2011;Nikolovski et al, 2012;Heard et al, 2015 At5g53010 Calciumtransporting ATPase, putative Ferro et al, 2010;Zybailov et al, 2008;Ferro et al, 2010;Tomizioli et al, 2014;Eisenhut et al, 2018;Zhang et al, 2018;Frank et Zhang et al, 2018). In addition to Ca 2+ channels and transporters, Ca 2+ sensors, namely 21 proteins, are predicted to be located in plastids.…”

Manganese Homeostasis in Cyanobacteria

“…Loss of the envelope localized CMT1 or thylakoid residing PAM71 resulted in strongly reduced loading of PSII with Mn. Obviously, the major substrate of both CMT1 and PAM71 is Mn [41,42]. Mn as the preferred substrate was also demonstrated for the homologous protein Mnx in Synechocystis.…”