The trans-Golgi-localized protein BICAT3 regulates manganese allocation and matrix polysaccharide biosynthesis

Abstract

Manganese (Mn2+) is essential for a diversity of processes, including photosynthetic water splitting and the transfer of glycosyl moieties. Various Golgi-localized glycosyltransferases that mediate cell wall matrix polysaccharide biosynthesis are Mn2+-dependent, but the supply of these enzymes with Mn2+ is not well understood. Here, we show that the BIVALENT CATION TRANSPORTER 3 (BICAT3) localizes specifically to trans-cisternae of the Golgi. In agreement with a role in Mn2+ and Ca2+ homeostasis, BICAT3 rescued yeast (Saccharomyces cerevisiae) mutants defective in their translocation. Arabidopsis (Arabidopsis thaliana) knockout mutants of BICAT3 were sensitive to low Mn2+ and high Ca2+ availability and showed altered accumulation of these cations. Despite reduced cell expansion and leaf size in Mn2+-deficient bicat3 mutants, their photosynthesis was improved, accompanied by an increased Mn content of chloroplasts. Growth defects of bicat3 corresponded with an impaired glycosidic composition of matrix polysaccharides synthesized in the trans-Golgi. In addition to the vegetative growth defects, pollen tube growth of bicat3 was heterogeneously aberrant. This was associated with a severely reduced and similarly heterogeneous pectin deposition and caused diminished seed set and silique length. Double mutant analyses demonstrated that the physiological relevance of BICAT3 is distinct from that of ER-TYPE CA2+-ATPASE 3 (ECA3), a Golgi-localized Mn2+/Ca2+-ATPase. Collectively, BICAT3 is a principal Mn2+ transporter in the trans-Golgi whose activity is critical for specific glycosylation reactions in this organelle and for the allocation of Mn2+ between Golgi apparatus and chloroplasts.

A Golgi-Located Transmembrane Nine Protein Gene TMN11 Functions in Manganese/Cadmium Homeostasis and Regulates Growth and Seed Development in Rice

“…Mutation of Golgi Mn transporters TM9SF4 (a V-type ATPase-associated protein belonging to the Golgi-resident TMN family member) and TMEM165 (Ca/Mn pump, a calcium-permeable channel), which are responsible for transport of Mn or other metals in or out of the Golgi, also cause dysfunctions in cell division and differentiation in mammalian cells that evoke pathogenesis and clinical diseases [ 17 , 30 , 32 , 33 ]. The importance of Golgi Mn homeostasis has also been demonstrated by several non-TM9 family transport proteins, such as AtMTP11 [ 25 ], OsMTP11 [ 34 , 35 , 36 ], PML3 (UPF0016) [ 37 ], BnMTP9 [ 38 ], and BICAT3 (BIVALENT CATION TRANSPORTER 3) [ 39 ], and disruption of these transport proteins can lead to impaired growth and development by blocking vesicle secretory pathways or cell wall polysaccharide biosynthesis under elevated or normal Mn supply conditions. These results strongly suggest that OsTMN11-mediated Mn homeostasis is also necessary to maintain the processing of growth-related proteins in the Golgi.…”

Manganese management in plants: Golgi transporter determines manganese allocation and cell wall composition

“…These cell wall defects in bicat3 are likely the result of reduced glycosyltransferase activity in the Golgi and suggest that other Mn 2+ -transport proteins, like ECA3, cannot (fully) replace BICAT3 function. Surprisingly, comparing bicat3 and eca3 plants, He et al 2022 found that photosynthesis was improved in eca3 in their hydroponic experimental set-up, albeit less pronounced than in bicat3 . This contrasts with previous findings using in vitro grown seedlings that show severely reduced chlorophyll content in eca3 ( Mills et al, 2008 ), suggesting decreased photosynthesis.…”

“… He et al (2022) found that the loss of BICAT3 led to higher Mn 2+ concentration in shoots under Mn deficiency, and photosynthesis was improved in bicat3 . Mn 2+ analysis of isolated chloroplasts revealed higher chloroplast Mn 2+ content, strongly suggesting that this is the reason for the higher overall shoot Mn 2+ concentration.…”

“…In this issue of Plant Physiology , ( He et al (2022) , characterized the Arabidopsis Bivalent Cation Transporter 3 (BICAT3) as a principal manganese transporter localized specifically in trans-Golgi cisternae ( Figure 1 ). They showed that BICAT3 is ubiquitously expressed in both areal and nonareal tissues, and that its function is crucial for pollen tube growth and for plant performance under Mn 2+ deficiency, confirming and expanding on previous work ( Hoecker et al, 2020 ; Zhang et al, 2021 ).…”

“…Additionally, bicat3 plants take up more Mn 2+ , which is allocated to chloroplasts, improving photosynthesis. Partly created using biorender, adapted from He et al (2022) .…”