A member of cation diffusion facilitator family, MTP11, is required for manganese tolerance and high fertility in rice

Abstract

Rice MTP11 is the trans-Golgi-localized transporter that is involved in Mn tolerance with MTP8.1, and it is required for normal fertility. Rice (Oryza sativa L.) is one of the most manganese (Mn)-tolerant species, and it is able to accumulate high levels of this metal in the leaves without showing toxic symptoms. The metal tolerance protein 8.1 (MTP8.1), a member of the Mn-cation diffusion facilitator (CDF) family, has been shown to play a central role in high Mn tolerance by sequestering Mn into vacuoles. Recently, rice MTP11 was identified as an Mn transporter that is localized to Golgi-associated compartments, but its exact role in Mn tolerance in planta has not yet been understood. Here, we investigated the role of MTP11 in rice Mn tolerance using knockout lines. Old leaves presented higher levels of constitutively expressed MTP11 than other tissues and MTP11 expression was also found in reproductive organs. Fused MTP11:green fluorescent protein was co-localized to trans-Golgi markers and differentiated from other Golgi-associated markers. Knockout of MTP11 in wild-type rice did not affect tolerance and accumulation of Mn and other heavy metals, but knockout in the mtp8.1 mutant showed exacerbated Mn sensitivity at the vegetative growth stage. Knockout of MTP11 alone resulted in decreased grain yield and fertility at the reproductive stage. Thus, MTP11 is a trans-Golgi localized transporter for Mn, which plays a role in Mn tolerance through intracellular Mn compartmentalization. It is also required for maintaining high fertility in rice.

Advances in the Mechanisms of Plant Tolerance to Manganese Toxicity

“…Therefore, a secretory pathway involving vesicular trafficking and exocytosis mediated by AtMTP11 is believed to help increase Mn tolerance in Arabidopsis [28]. Similar functions of other MTPs in sequestering Mn into the Golgi apparatus have been reported for OsMTP11 from rice [27], HvMTP8.1 and HvMTP8.2 from barley [77], PtMTP11.1 and PtMTP11.2 from poplar ( Populus trichocarpa ) [28], as well as BmMTP10 and BmMTP11 from beets ( Beta vulgaris ) [78].…”

“…For example, activation of the antioxidant system, including the free radical-mitigating antioxidant enzymes and nonenzymatic components, is thought to be vital for plants alleviating excess Mn-induced oxidative stress [25]. The important roles of the regulation of Mn uptake, translocation, and distribution have been implicated in many plants’ responses to Mn toxicity, such as rice ( Oryza sativa ) [26,27], Arabidopsis ( Arabidopsis thaliana ) [28], and Caribbean stylo ( Stylosanthes hamata ) [29]. Furthermore, plants can sequester Mn into subcellular compartments, such as vacuoles, the endoplasmic reticulum (ER), Golgi apparatuses, and cell walls, to withstand the toxic effects of high Mn stress [30,31].…”

Genome-Wide Identification, Comprehensive Gene Feature, Evolution, and Expression Analysis of Plant Metal Tolerance Proteins in Tobacco Under Heavy Metal Toxicity

“…Both OsMTP8.1 and OsMTP8.2 were tonoplast-localized Mn transporters, and OsMTP9 was involved in efficient root Mn uptake (Chen et al, 2013; Ueno et al, 2015; Takemoto et al, 2017; Tsunemitsu et al, 2018b). Moreover, OsMTP11 played a crucial role in Mn tolerance through intracellular Mn compartmentalization, although the correct localization of this protein was still under debate (Farthing et al, 2017; Zhang and Liu, 2017; Ma et al, 2018; Tsunemitsu et al, 2018a). In addition, some MTP proteins from cucumber were recently isolated and their corresponding substrates were also specified.…”

Physiological responses and proteomic changes reveal insights into Stylosanthes response to manganese toxicity

“…For example, loss-of-function analyses of metal tolerance protein (MTP) demonstrate the importance of Mn sequestration into vacuoles in Mn tolerance in rice ( Oryza sativa ) and Arabidopsis [20, 21]. Recently, it has been shown that sequestration of Mn into Golgi-associated compartments by the function of OsMTP11 is also important for Mn homeostasis in rice [22]. Additionally, organic acids exuded from the root apex can chelate Mn, thereby alleviating Mn toxicity via decreasing Mn uptake by the roots [23–25].…”