Dimethylarsinic acid is the causal agent inducing rice straighthead disease

Abstract

Straighthead disease is a physiological disorder in rice with symptoms of sterile spikelets, distorted husks, and erect panicles. Methylated arsenic species have been implicated as the causal agent of the disease, but direct evidence is lacking. Here, we investigated whether dimethylarsinic acid (DMA) causes straighthead disease and its effect on the transcriptome of young panicles. DMA addition caused typical straighthead symptoms in hydroponic culture, which were alleviated by silicon addition. DMA addition to soil at the tillering to flowering stages induced straighthead disease. Transgenic rice expressing a bacterial arsenite methyltransferase gene gained the ability to methylate arsenic to mainly DMA, with the consequence of inducing straighthead disease. Field surveys showed that seed setting rate decreased with increasing DMA concentration in the husk, with an EC50 of 0.18 mg kg−1. Transcriptomic analysis showed that 364 and 856 genes were significantly up- and down-regulated, respectively, in the young panicles of DMA-treated plants compared with control, whereas Si addition markedly reduced the number of genes affected. Among the differentially expressed genes, genes related to cell wall modification and oxidative stress responses were the most prominent, suggesting that cell wall metabolism is a sensitive target of DMA toxicity and silicon protects against this toxicity.

Relationships Among Arsenic-Related Traits, Including Rice Grain Arsenic Concentration and Straighthead Resistance, as Revealed by Genome-Wide Association

“…Because StHD has been attributed to As toxicity (Tang et al, 2020a), to explore candidate genes underlying the 23 StHD RMC GWA-QTL ( (Sze et al, 1992;Lüttge and Ratajczak, 1997). Furthermore, ATX1 is known to interact with heavy metal P1B-ATPases, suggesting its role in delivering Cu to heavy metal P1B-ATPases for Cu trafficking and distribution in order to maintain Cu homeostasis in rice (Zhang et al, 2018).…”

“…As exposure is known to reduce root and shoot growth (Heuschele et al, 2017;Kalita et al, 2018;Murugaiyan et al, 2019) and has long been associated with a physiological disorder in rice known as straighthead (StHD), so called because it is characterized by erect seed heads (panicles) upon maturity from poor seed set in often distorted spikelets. While direct evidence documenting the oAs DMA as the cause of StHD was only recently determined (Tang et al, 2020a), herbicides containing the synthetic oAs monosodium methanearsonate (MSMA) have been used for decades to induce StHD for the purpose of facilitating selection of StHD-resistant breeding progeny (Yan et al, 2005). Plant genes and mechanisms that reduce As uptake or enhance As detoxification by chelation and/or vacuolar sequestration would be expected to reduce both grain-As and the severity of As-induced plant stress, such as StHD.…”

The roles of membrane transporters in arsenic uptake, translocation and detoxification in plants

“…Although it is generally thought that pentavalent MMAs and DMAs are less toxic to mammals and humans than inorganic As (Hirano et al, 2004;, DMAs is actually more toxic to plants than inorganic As (Tang, Kang et al, 2016). In addition, DMAs is suspected to be the causal agent of rice straighthead disease (Limmer et al, 2018;Tang et al, 2020;Zheng et al, 2013). Some microorganisms are able to methylate As(III) to mono-, di-or tri-methyl arsenic species via the enzyme As(III) S-adenosylmethionine methyltransferase (ArsM) (Qin et al, 2006;2009;Ye et al, 2012).…”

Identification of Promising Genotypes Through Systematic Evaluation for Arsenic Tolerance and Exclusion in Rice (Oryza sativa L.)

“…As toxicity in rice plants has a cascade effect that includes preventing the most sensitive germination phase, limiting cell division, elongation of the primary roots, stunted development, and, finally, grain accumulation (Suriyagoda et al, 2018;Murugaiyan et al, 2021). As absorption by the roots and transport to the leaves via the transpiration stream via xylem resulting in a toxic As load in plant tissues (Tang et al, 2020). The presence of arsenic toxicity characteristics in rice germplasm under our experimental circumstances indicates that As tolerance and accumulation in rice is a quantitatively inherited trait influenced by multiple factors.…”

“…Arsenic dynamics in these conditions are poorly understood and no suitable rice varieties for Ascontaminated regions have been identified. For DSR production systems, the presence of inorganic As in the soil may significantly affect the most sensitive seed germination and establishment processes (Tang et al, 2020). When rice is grown in the monsoon wet season, dry-seeded rice is likely to be flooded (anaerobic conditions) most of the time.…”