Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance

Authors: Liu, Jiping; SIVAGURU, MAYANDI - University Of Illinois; Kochian, Leon

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/12/2013
Publication Date: 7/19/2013
Citation: Liu, J., Sivaguru, M., Kochian, L.V. 2013. Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance. Plant Journal. DOI: 10.1111/tpj.12290.

Interpretive Summary: Over 20% of the US land area and approximately 50% of the world’s arable lands are acidic (pH < 5). On these acid soils, aluminum (Al) toxicity is the primary factor limiting agricultural productivity, as toxic Al results in damaged and stunted plant root systems, ultimately resulting in a reduction of crop yields. Given that a large proportion of the acid soils are found in the tropics/subtropics regions where many developing countries are located, Al toxicity limits agricultural productivity in the very areas where food security is most tenuous. Because of the importance of this problem to agriculture worldwide, there is considerable interest and research effort by researchers at universities, government agencies, and international agriculture organizations in identifying genes that provide tolerance to Al toxicity in order to improve crop Al tolerance via molecular breeding and biotechnology. The release of organic acid from the root apex in response to Al-stress constitutes a widespread Al-tolerance mechanism by which plant roots are able to ameliorate the toxic levels of Al surrounding the growing root, as the released organic acid binds and detoxifies the Al ions. We previously identified a major Al tolerance gene in sorghum, SbMATE, which encodes a root tip citrate efflux transporter. Citrate is a very important carbon compound to plants; hence, its release into the soil is costly to the plant. In the current study, we show that the SbMATE gene and protein are only expressed in the very root cells which are most damaged by Al, which is a region 1-3 mm behind the root tip. Also, SbMATE is only expressed in the two outer cell layers in this discrete band of the root tip. Hence, Al-resistant sorghum plants have evolved an effective strategy to precisely localize root citrate exudation to the specific site of greatest Al induced root damage, which minimizes plant carbon loss while maximizing protection of the root cells most susceptible to Al-damage.

Technical Abstract: Aluminum (Al) toxicity is one of the major limiting factors for crop production on acid soils that comprise significant portions of the world’s lands. Al resistance in the cereal crop, Sorghum bicolor, is mainly achieved by Al-activated root apical citrate exudation, which is mediated by the plasma membrane localized citrate efflux transporter encoded by SbMATE. Here we precisely localize tissue- and cell-specific Al toxicity responses as well as SbMATE gene and protein expression in root tips of an Al-resistant near-isogenic-line (NIL). We found that Al induced the greatest cell damage and generation of reactive oxygen species specifically in the root distal transition-zone (DTZ), a region 1-3 mm behind the root tip where transition from cell division to cell elongation occurs. These findings indicate that the root DTZ is the primary region of root Al stress. Furthermore, Al-induced SbMATE gene and protein expression were specifically localized to the epidermal and outer cortical cell layers of the DTZ in the Al-resistant NIL, and the process was precisely coincident with the time course of Al induction of SbMATE expression and the onset of the recovery of roots from Al-induced damage. These findings show that SbMATE gene and protein expression are induced when and where the root cells experience the greatest Al stress. Hence, Al-resistant sorghum plants have evolved an effective strategy to precisely localize root citrate exudation to the specific site of greatest Al induced root damage, which minimizes plant carbon loss while maximizing protection of the root cells most susceptible to Al-damage.