|ARBELAEZ, JUAN - Cornell University|
|MARON, LYZA - Cornell University|
|JOBE, TIMOTHY - Boyce Thompson Institute|
|REBELO, ANA - Cornell University|
|FAMOSO, ADAM - Cornell University|
|MA, QIYUE - Boyce Thompson Institute|
|FEI, ZHANGJUN - Boyce Thompson Institute|
|KOCHIAN, LEON - Former ARS Employee|
|MCCOUCH, SUSAN - Cornell University|
Submitted to: Plant and Soil
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/14/2017
Publication Date: 10/16/2017
Citation: Arbelaez, J., Maron, L., Jobe, T., Pineros, M., Rebelo, A., Famoso, A., Ma, Q., Fei, Z., Kochian, L., McCouch, S. 2017. Aluminum resistance transcription factor 1 (ART1) contributes to natural variation in rice aluminum resistance. Plant and Soil. 1(4):1-19. https://doi.org/10.1002/pld3.14.
Interpretive Summary: Approximately 50% of the world's arable lands, including over one fifth of the US lands, are acidic (pH < 5). In these soils, aluminum (Al) toxicity results in damaged and stunted plant root systems, causing a reduction of crop yields, thereby constituting the primary factor limiting agricultural productivity in geographical areas where food security is most tenuous. These limitations have led research efforts at universities, government agencies, and international agriculture organizations to identifying genes involved in providing resistance to Al toxicity, as means to improve crop Al tolerance via molecular breeding and biotechnology. The understanding of the molecular mechanism(s) involved in perceiving Al-stress and relaying this information to achieve proper regulation of genes related to Al-resistance processes is limited. In this study we used genetic, physiological and molecular approaches to understand the impact that natural variation and genetic background has on ART1 (a regulator factor controlling the expression of Al-resistance related genes). We showed that ART1 regulates the expression of a more complex suite of genes than previously thought and its efficiency is greatly dependent on the genetic background composition. These findings explain why the transfer of a single gene (as exemplified with ART1) to Al sensitive crop varieties is not sufficient to provide higher levels of Al resistance. Understanding of the various elements involved in the complex network of Al-resistance responses is fundamental to guide future genetic studies and breeding efforts aimed at generating an efficient crop improvement for agriculture on acid soils.
Technical Abstract: Transcription factors (TFs) mediate stress resistance indirectly via physiological mechanisms driven by the array of genes they regulate. Therefore, when studying TF-mediated stress resistance, it is important to understand how TFs interact with different genetic backgrounds. Here, we fine-mapped the major aluminum (Al) resistance QTL Alt12.1 to a 44 Kb region surrounding ART1, which encodes a C2H2-type zinc finger TF required for Al resistance in rice. The parents of the mapping population Al-resistant Azucena (tropical japonica) and Al-sensitive IR64 (indica) showed similar ART1 expression levels but extensive sequence polymorphism within the ART1 coding region. Using reciprocal near-isogenic lines (NILs) in the Azucena and IR64 genetic backgrounds, we examined how allele-swapping Alt12.1 would affect plant responses to Al. Analysis of global transcriptional responses to Al stress in roots of the reciprocal NILs alongside their recurrent parents demonstrated that the ART1 from Al-resistant Azucena led to greater changes in gene expression in response to Al when compared to the ART1 from IR64 in both genetic backgrounds. The presence of the ART1 allele from the opposite parent affected the expression of several genes not previously implicated in rice Al tolerance. We also highlight specific examples where putatively functional variation in cis-regulatory regions of ART1-regulated genes interacts with ART1 to determine gene expression in response to Al. This ART1-promoter interaction is associated with transgressive variation for Al resistance in the Azucena x IR64 population. These results illustrate how ART1 interacts with the genetic background in determining quantitative phenotypic variation in rice Al resistance.