Relationships among arsenic-related traits, including grain arsenic concentration and rice straighthead resistance, as revealed by genome-wide association

Authors: Pinson, Shannon; Heuschele, Deborah - Jo; Edwards, Jeremy; Jackson, Aaron; Sharma, Santosh; Barnaby, Jinyoung

Submitted to: Frontiers in Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/23/2021
Publication Date: 3/14/2022
Citation: Pinson, S.R., Heuschele, D.J., Edwards, J., Jackson, A.K., Sharma, S., Barnaby, J.Y. 2022. Relationships among arsenic-related traits, including grain arsenic concentration and rice straighthead resistance, as revealed by genome-wide association. Frontiers in Genetics. https://doi.org/10.3389/fgene.2021.787767.
DOI: https://doi.org/10.3389/fgene.2021.787767

Interpretive Summary: There is global concern about the level of arsenic contained in rice grains. While a survey by the US FDA of more than 1000 samples of rice and rice products produced in the USA determined that US-produced rice is safe for human consumption, only a portion of their samples met the more stringent, lower limit on arsenic required for baby foods. Arsenic is of higher concern in rice than other grain crops because rice is typically produced under flooded field conditions, creating an environment that makes some compounds, including arsenic, more available for plant uptake. Arsenic is also toxic to plants, and causes a disorder in rice known as straighthead, so named because it reduces grain production to the degree that the sterile (seedless) panicles remain erect rather than bending over due to weight of grains. We know that some rice varieties are more susceptible to straighthead than others, and existence of genetic variation in straighthead resistance suggests that rice has evolved genes and mechanisms that reduce the arsenic toxicity in some way. For example, either through reduced arsenic uptake, or detoxification inside the plant. Because these mechanisms would also be expected to reduce the accumulation of arsenic in rice grains, we hypothesized that some mapped genes/QTLs affecting straighthead would also impact grain-arsenic. Because silica and phosphorus are known to affect arsenic uptake, while sulfur, calcium, and copper can reduce cellular damage from arsenic toxicity, we identified and compared the chromosomal locations of genes affecting these elements as well. While we did find some shared straightead and arsenic related genes, they were not as common as our hypothesis predicted. We had also predicted that we would find silica to be more commonly associated with arsenic genes than with straighthead genes because we hypothesized that silica would impact straighthead by first affecting arsenic uptake. Once again, our results were contrary to our hypothesis, and we found numerous instances where straighthead and silica genes coincided but without a coincident effect on arsenic. These results indicate that straighthead resistance involves some mechanisms that affect grain arsenic, but involves additional mechanisms independent of arsenic. The frequency of co-location of straighthead and silica QTLs further indicates that silica might be causing some of these non-arsenic associations. It is known that silica can enhance the ability of plants to uptake elements in addition to arsenic. Silica is also known to help plants produce antioxidants, which help reduce cell damage caused by the reactive oxygen species (ROS) that otherwise accumulate in stressed cells and plants. Thus, the genes/QTL we did fine for arsenic, straighthead, and silica in rice remain useful to breeders and scientists desiring to create new rice varieties with improved grain nutritional value as well as increased resistance to straighthead disorder.

Technical Abstract: There is global concern that rice grains and foods can contain harmful amounts of arsenic (As), motivating breeders to produce cultivars that restrict As accumulation in grains to protect human health. Arsenic is also toxic to plants, with straighthead disorder (StHD), causing panicle sterility, being observed in rice. Genetic variation in StHD resistance suggests that plants have evolved mechanisms that reduce As toxicity, possibly via regulation of As uptake, transport, or detoxification/sequestration. Because these mechanisms could also underlie the wide (3 to 100-fold) differences in grain-As observed among diverse rice genotypes, it was hypothesized that some genes reduce both grain-As content and StHD susceptibility, and maybe detectable as co-located StDH and As quantitative trait loci (QTL). We used a machine-learning Bayesian network approach along with high resolution genome wide association study (GWAS) to identify QTL for grain-As and StHD resistance within the USDA Rice Minicore Collection (RMC). Arsenic enters roots through phosphorus (P) and silica (Si) transporters, As-detoxification involves S, and cell signaling to to tolerate abiotic stress is impacted by Si, Ca, and Cu. Therefore, concentrations of Si, P, S, Ca, and Cu were included in this study to elucidate physiological mechanisms underlying grain-As and StHD QTL. Multiple QTL (from 9 to 33) were identified for each of the investigated As-associated traits. Although the QTL we identified for StHD, grain-As and hull-Si were not as overlapped as our hypothesis predicted (4/33 StHD and 4/15 As QTL co-located), they do provide useful guidance to future research. Furthermore, these are the first StHD and Si QTL to be identified using high-density mapping, resulting in their being mapped to shorter, more precise genomic regions than previously reported QTL. The candidate genes identified also provide guidance for future research, such as gene editing or mutation studies to further investigate the role antioxidants and improved ROS scavenging to StHD resistance, as indicated by candidate genes around qStHD8-2, and as has been documented for other abiotic stresses. Other genes indicated for future study for improving grain-As and StHD include several Multidrug And Toxin Efflux (MATE) genes, F-box genes, and NIPs not documented to date to transport As.