Dataset Information

Seeing red: the origin of grain pigmentation in US weedy rice.

ABSTRACT: Weedy forms of crop species infest agricultural fields worldwide and are a leading cause of crop losses, yet little is known about how these weeds evolve. Red rice (Oryza sativa), a major weed of cultivated rice fields in the US, is recognized by the dark-pigmented grain that gives it its common name. Studies using neutral molecular markers have indicated a close relationship between US red rice and domesticated rice, suggesting that the weed may have originated through reversion of domesticated rice to a feral form. We have tested this reversion hypothesis by examining molecular variation at Rc, the regulatory gene responsible for grain pigmentation differences between domesticated and wild rice. Loss-of-function mutations at Rc account for the absence of proanthocyanidin pigments in cultivated rice grains, and the major rc domestication allele has been shown to be capable of spontaneous reversion to a functional form through additional mutations at the Rc locus. Using a diverse sample of 156 weedy, domesticated and wild Oryzas, we analysed DNA sequence variation at Rc and its surrounding 4 Mb genomic region. We find that reversion of domestication alleles does not account for the pigmented grains of weed accessions; moreover, we find that haplotypes characterizing the weed are either absent or very rare in cultivated rice. Sequences from genomic regions flanking Rc are consistent with a genomic footprint of the rc selective sweep in cultivated rice, and they are compatible with a close relationship of red rice to Asian Oryzas that have never been cultivated in the US.

SUBMITTER: Gross BL

PROVIDER: S-EPMC2921015 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Seeing red: the origin of grain pigmentation in US weedy rice.

Gross Briana L BL Reagon Michael M Hsu Shih-Chung SC Caicedo Ana L AL Jia Yulin Y Olsen Kenneth M KM

Molecular ecology 20100624 16

Weedy forms of crop species infest agricultural fields worldwide and are a leading cause of crop losses, yet little is known about how these weeds evolve. Red rice (Oryza sativa), a major weed of cultivated rice fields in the US, is recognized by the dark-pigmented grain that gives it its common name. Studies using neutral molecular markers have indicated a close relationship between US red rice and domesticated rice, suggesting that the weed may have originated through reversion of domesticated ...[more]

PMID: 20584133

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Project description:Background: Weedy rice (Oryza sativa L.) is a worldwide problem in rice production, being highly tolerant to sub-optimal nutrient levels hence competitive in nutrient acquisition. To understand the function of genes that are potentially involved in the high nutrient acquisition ability of weedy rice, we compared the transcriptomes of strawhull weedy red rice (tolerant to N deficit) with the rice cultivar ‘Wells’ (intolerant to N deficit), by examining profiles in flag leaves at panicle initiation under low and optimum N levels. Strawhull weedy red rice and cultivar ‘Wells’ were grown in nutrient solution with NH4NO3 concentration manipulated to simulate optimum and deficient N conditions. Changes in gene expression in leaf tissues were analyzed at three conditions: N deficiency, and at 24- and 48-h NH4NO3 supplementation after N starvation. Differential gene expression on weedy red rice was evaluated using oligonucleotide arrays representing 44,974 rice gene models. Overall, comparative real-time PCR analysis of 21 candidate genes identified from the microarray data between weedy red rice and cultivar ‘Wells’ supported our hypothesis that key genes involved in N assimilation are expressed differentially at N- deficient conditions between the tolerant and intolerant strains. Results: Eight candidate genes showed significant differences in expression at one of the time points: N and starch metabolism-related [alanine aminotransferase (OsAlaAT) locus ID Os10g25140.1; soluble starch synthase 2-1(OsSSSII1), Os10g30156.1; and soluble starch synthase 2-3(OsSSSII3), Os06g12450.1]; cell structure-related [alpha-L-fucosidase 2 precursor (OsFUCA2), Os06g06250.1]; signal transduction [two-component response regulator-like(OsPRR1), Os02g40510.1 and EF hand family protein (OsPOLC2_JUNOX), Os02g50060.1]; and transcription factors [zinc finger, C2H2 type family protein(OsC2H2Znf), Os11g06840.1 and Myb-like DNA-binding domain (OsMYB), Os01g62660.1]. Genome-wide gene expression analysis of weedy rice showed that nitrite reductase (Os01g25484.1; Os01g25484.2; Os01g25484.3) was most highly induced at N starvation and was most deeply repressed at 24 h of N-stress recovery. A few other genes, namely SANT/MYB (Os01g47370.1), chaperonin (Os02g54060.1; Os02g54060.2), protein phosphatase (Os09g15670.1), polyamine transporter (Os01g61044.1), trehalose-6-phosphate synthase (Os02g54820.2), uracil phosphoribosyltransferase (Os05g38170.1), an MIKCc type-box transcription factor (Os02g52340.1), a cell homeostasis-related uncharacterized protein (Os02g16880.1), a protease inhibitor (Os07g18990.1), dehydrin (Os11g26760.1), and cytochrome P450 (Os11g05380.1) were also strong indicators of starvation and recovery. Conclusions: Weedy rice has N-stress adaptive mechanisms that are probably distinct to the mechanisms in most cultivars. This mechanism potentially contributes to its high vigor and competitive advantage over most rice cultivars under sub-optimal nutrient levels. Expression of key genes involved in nitrate assimilation, trehalose synthesis, and protein modification appeared to be critical for adaptation to N stress in weedy rice. N-stress tolerance of weedy red rice appeared to be due at least in part to the ability to sustain C fixation and starch synthesis during N starvation.

Project description:Background: Weedy rice (Oryza sativa L.) is a worldwide problem in rice production, being highly tolerant to sub-optimal nutrient levels hence competitive in nutrient acquisition. To understand the function of genes that are potentially involved in the high nutrient acquisition ability of weedy rice, we compared the transcriptomes of strawhull weedy red rice (tolerant to N deficit) with the rice cultivar M-bM-^@M-^XWellsM-bM-^@M-^Y (intolerant to N deficit), by examining profiles in flag leaves at panicle initiation under low and optimum N levels. Strawhull weedy red rice and cultivar M-bM-^@M-^XWellsM-bM-^@M-^Y were grown in nutrient solution with NH4NO3 concentration manipulated to simulate optimum and deficient N conditions. Changes in gene expression in leaf tissues were analyzed at three conditions: N deficiency, and at 24- and 48-h NH4NO3 supplementation after N starvation. Differential gene expression on weedy red rice was evaluated using oligonucleotide arrays representing 44,974 rice gene models. Overall, comparative real-time PCR analysis of 21 candidate genes identified from the microarray data between weedy red rice and cultivar M-bM-^@M-^XWellsM-bM-^@M-^Y supported our hypothesis that key genes involved in N assimilation are expressed differentially at N- deficient conditions between the tolerant and intolerant strains. Results: Eight candidate genes showed significant differences in expression at one of the time points: N and starch metabolism-related [alanine aminotransferase (OsAlaAT) locus ID Os10g25140.1; soluble starch synthase 2-1(OsSSSII1), Os10g30156.1; and soluble starch synthase 2-3(OsSSSII3), Os06g12450.1]; cell structure-related [alpha-L-fucosidase 2 precursor (OsFUCA2), Os06g06250.1]; signal transduction [two-component response regulator-like(OsPRR1), Os02g40510.1 and EF hand family protein (OsPOLC2_JUNOX), Os02g50060.1]; and transcription factors [zinc finger, C2H2 type family protein(OsC2H2Znf), Os11g06840.1 and Myb-like DNA-binding domain (OsMYB), Os01g62660.1]. Genome-wide gene expression analysis of weedy rice showed that nitrite reductase (Os01g25484.1; Os01g25484.2; Os01g25484.3) was most highly induced at N starvation and was most deeply repressed at 24 h of N-stress recovery. A few other genes, namely SANT/MYB (Os01g47370.1), chaperonin (Os02g54060.1; Os02g54060.2), protein phosphatase (Os09g15670.1), polyamine transporter (Os01g61044.1), trehalose-6-phosphate synthase (Os02g54820.2), uracil phosphoribosyltransferase (Os05g38170.1), an MIKCc type-box transcription factor (Os02g52340.1), a cell homeostasis-related uncharacterized protein (Os02g16880.1), a protease inhibitor (Os07g18990.1), dehydrin (Os11g26760.1), and cytochrome P450 (Os11g05380.1) were also strong indicators of starvation and recovery. Conclusions: Weedy rice has N-stress adaptive mechanisms that are probably distinct to the mechanisms in most cultivars. This mechanism potentially contributes to its high vigor and competitive advantage over most rice cultivars under sub-optimal nutrient levels. Expression of key genes involved in nitrate assimilation, trehalose synthesis, and protein modification appeared to be critical for adaptation to N stress in weedy rice. N-stress tolerance of weedy red rice appeared to be due at least in part to the ability to sustain C fixation and starch synthesis during N starvation. Plants were subjected to four treatments: T1 M-bM-^@M-^S Full N; T2 M-bM-^@M-^S NH4NO3starvation until NSI <95%; T3 - 24-h NH4NO3 readdition post-starvation; and T4 M-bM-^@M-^S 48-h NH4NO3 readdition post-starvation. The 24- and 48-h time points for NH4NO3 supplementation were selected to assess both the early and late molecular responses. There were four replications, with three plants per replication per N treatment.

Project description:Domestication is the hallmark of evolution and civilization and harnesses biodiversity through selection for specific traits. In regions where domesticated lines are grown near wild relatives, congeneric sources of aggressive weedy genotypes cause major economic losses. Thus, the origins of weedy genotypes where no congeneric species occur raise questions regarding management effectiveness and evolutionary mechanisms responsible for weedy population success. Since eradication in the 1970s, California growers avoided weedy rice through continuous flood culture and zero-tolerance guidelines, preventing the import, presence, and movement of weedy seeds. In 2003, after decades of no reported presence in California, a weedy rice population was confirmed in dry-seeded fields. Our objectives were to identify the origins and establishment of this population and pinpoint possible phenotypes involved. We show that California weedy rice is derived from a different genetic source among a broad range of AA genome Oryzas and is most recently diverged from O. sativa temperate japonica cultivated in California. In contrast, other weedy rice ecotypes in North America (Southern US) originate from weedy genotypes from China near wild Oryza, and are derived through existing crop-wild relative crosses. Analyses of morphological data show that California weedy rice subgroups have phenotypes like medium-grain or gourmet cultivars, but have colored pericarp, seed shattering, and awns like wild relatives, suggesting that reversion to non-domestic or wild-like traits can occur following domestication, despite apparent fixation of domestication alleles. Additionally, these results indicate that preventive methods focused on incoming weed sources through contamination may miss burgeoning weedy genotypes that rapidly adapt, establish, and proliferate. Investigating the common and unique evolutionary mechanisms underlying global weed origins and subsequent interactions with crop relatives sheds light on how weeds evolve and addresses broader questions regarding the stability of selection during domestication and crop improvement.

Dataset Information

Seeing red: the origin of grain pigmentation in US weedy rice.

Publications

Seeing red: the origin of grain pigmentation in US weedy rice.

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