SignificanceFlowering time is a critical determinant of crop adaptation to local environments. As a result of natural and artificial selection, maize has evolved a reduced photoperiod sensitivity to adapt to regions over 90° of latitude in the Americas. Here we show that a distant Harbinger-like transposon acts as a cis-regulatory element to repress ZmCCT9 expression to promote flowering under the long days of higher latitudes. The transposon at ZmCCT9 and another functional transposon at a second flowering-time gene, ZmCCT10, arose sequentially following domestication and were targeted by selection as maize spread from the tropics to higher latitudes. Our results demonstrate that new functional variation created by transposon insertions helped maize to spread over a broad range of latitudes rapidly.
Increased planting densities have boosted maize yields. Upright plant architecture facilitates dense planting. Here, we cloned UPA1 (Upright Plant Architecture1) and UPA2, two quantitative trait loci conferring upright plant architecture. UPA2 is controlled by a two-base sequence polymorphism regulating the expression of a B3-domain transcription factor (ZmRAVL1) located 9.5 kilobases downstream. UPA2 exhibits differential binding by DRL1 (DROOPING LEAF1), and DRL1 physically interacts with LG1 (LIGULELESS1) and represses LG1 activation of ZmRAVL1. ZmRAVL1 regulates brd1 (brassinosteroid C-6 oxidase1), which underlies UPA1, altering endogenous brassinosteroid content and leaf angle. The UPA2 allele that reduces leaf angle originated from teosinte, the wild ancestor of maize, and has been lost during maize domestication. Introgressing the wild UPA2 allele into modern hybrids and editing ZmRAVL1 enhance high-density maize yields.
Summary The number of leaves and their distributions on plants are critical factors determining plant architecture in maize (Zea mays), and leaf number is frequently used as a measure of flowering time, a trait that is key to local environmental adaptation.Here, using a large set of 866 maize‐teosinte BC 2S3 recombinant inbred lines genotyped by using 19 838 single nucleotide polymorphism markers, we conducted a comprehensive genetic dissection to assess the genetic architecture of leaf number and its genetic relationship to flowering time.We demonstrated that the two components of total leaf number, the number of leaves above (LA) and below (LB) the primary ear, were under relatively independent genetic control and might be subject to differential directional selection during maize domestication and improvement. Furthermore, we revealed that flowering time and leaf number are commonly regulated at a moderate level. The pleiotropy of the genes ZCN8, dlf1 and ZmCCT on leaf number and flowering time were validated by near‐isogenic line analysis. Through fine mapping, qLA1‐1, a major‐effect locus that specifically affects LA, was delimited to a region with severe recombination suppression derived from teosinte.This study provides important insights into the genetic basis of traits affecting plant architecture and adaptation. The genetic independence of LA from LB enables the optimization of leaf number for ideal plant architecture breeding in maize.
Summary Maize (Zea mays) tassels underwent profound morphological changes during maize domestication and improvement. Although a number of genes affecting maize inflorescence development have been identified, the genetic basis of the morphological changes in maize tassels since domestication is not well understood.Here, using a large population of 866 maize‐teosinte BC 2S3 recombinant inbred lines genotyped using 19 838 single nucleotide polymorphism (SNP) markers, we performed high‐resolution quantitative trait locus (QTL) mapping for five tassel morphological traits.We showed that the five tassel traits were associated with different genetic architecture features. Known genes for maize inflorescence development identified by mutagenesis were significantly enriched in the tassel trait QTLs, and many of these genes, including ramosa1 (ra1), barren inflorescence2 (bif2), unbranched2 (ub2), zea floricaula leafy2 (zfl2) and barren stalk fastigiate1 (baf1), showed evidence of selection. An in‐depth nucleotide diversity analysis at the bif2 locus identified strong selection signatures in the 5′‐regulatory region. We also found that several known flowering time genes co‐localized with tassel trait QTLs. A further association analysis indicated that the maize photoperiod gene ZmCCT was significantly associated with tassel size variation. Using near‐isogenic lines, we narrowed down a major‐effect QTL for tassel length, qTL9‐1, to a 513‐kb physical region.These results provide important insights into the genetic architecture that controls maize tassel evolution.
Peripheral nerve injury causes neuropathic pain and microglia activation. P2Y12 receptors on microglia are thought to be a key player in the surveillance of the local environment, but whether or how these receptors are engaged in the cross-talk between microglia and neurons of the dorsal horn remain ambiguous. Using a rodent model of nerve injury-induced pain, we investigated the roles of P2Y12 in microglia activation, excitatory synaptic transmission, and nociceptive allodynia. We found that spinal nerve ligation (SNL) significantly increased the level of P2Y12 receptors specifically in the microglia of the ipsilateral dorsal horn. Injections of P2Y12 antagonists (MRS2395 or clopidogrel) attenuated microglia activation and increased the paw withdrawal latency in response to thermal stimuli on the ipsilateral side without affecting the basal threshold on the contralateral side. These effects on pain behaviors were replicated in P2Y12 knockout mice. Patch-clamp recordings further revealed that partial sciatic nerve ligation (PSNL)-induced excessive miniature excitatory postsynaptic currents (mEPSCs) were significantly attenuated in P2Y12 knockout mice. Moreover, we found that SNL activates the GTP-RhoA/ROCK2 signaling pathway and elevates the level of phosphorylated p38 mitogen-activated protein kinase (MAPK), which was inhibited by the P2Y12 antagonist. The phosphorylation of p38 MAPK was inhibited by a ROCK inhibitor, but not vice versa, suggesting that p38 MAPK is downstream of ROCK activation. Our findings suggest that nerve injury engages the P2Y12 receptor-dependent GTP-RhoA/ROCK2 signaling pathway to upregulate excitatory synaptic transmission in the dorsal horn. This cross-talk ultimately participates in the manifestation of nociceptive allodynia, implicating P2Y12 receptor as a potential target for alleviating neuropathic pain.
Studies that investigated the genetic basis of source and sink related traits have been widely conducted. However, the vascular system that links source and sink received much less attention. When maize was domesticated from its wild ancestor, teosinte, the external morphology has changed dramatically; however, less is known for the internal anatomy changes. In this study, using a large maize‐teosinte experimental population, we performed a high‐resolution quantitative trait locus (QTL) mapping for the number of vascular bundle in the uppermost internode of maize stem. The results showed that vascular bundle number is dominated by a large number of small‐effect QTLs, in which a total of 16 QTLs that jointly accounts for 52.2% of phenotypic variation were detected, with no single QTL explaining more than 6% of variation. Different from QTLs for typical domestication traits, QTLs for vascular bundle number might not be under directional selection following domestication. Using Near Isogenic Lines (NILs) developed from heterogeneous inbred family (HIF), we further validated the effect of one QTL qVb9‐2 on chromosome 9 and fine mapped the QTL to a 1.8‐Mb physical region. This study provides important insights for the genetic architecture of vascular bundle number in maize stem and sets basis for cloning of qVb9‐2.
Alternative splicing (AS) enhances transcriptome diversity and plays important roles in regulating plant processes. Although widespread natural variation in AS has been observed in plants, how AS is regulated and contribute to phenotypic variation is poorly understood. Here, we report a population-level transcriptome assembly and genome-wide association study to identify splicing quantitative trait loci (sQTLs) in developing maize () kernels from 368 inbred lines. We detected 19,554 unique sQTLs for 6570 genes. Most sQTLs showed small isoform usage changes without involving major isoform switching between genotypes. The sQTL-affected isoforms tend to display distinct protein functions. We demonstrate that nonsense-mediated mRNA decay, microRNA-mediated regulation, and small interfering peptide-mediated peptide interference are frequently involved in sQTL regulation. The natural variation in AS and overall mRNA level appears to be independently regulated with different -sequences preferentially used. We identified 214 putative-acting splicing regulators, among which , encoding an hnRNP-like glycine-rich RNA binding protein, regulates the largest-cluster. Knockout of by CRISPR/Cas9 altered splicing of numerous downstream genes. We found that 739 sQTLs colocalized with previous marker-trait associations, most of which occurred without changes in overall mRNA level. Our findings uncover the importance of AS in diversifying gene function and regulating phenotypic variation.
Maize (Zea mays) originated in tropical areas and is thus susceptible to low temperatures, which pose a major threat to maize production. Our understanding of the molecular basis of cold tolerance in maize is limited. Here, we identified bZIP68, a basic leucine zipper (bZIP) transcription factor, as a negative regulator of cold tolerance in maize. Transcriptome analysis revealed that bZIP68 represses the cold-induced expression of DREB1 transcription factor genes. The stability and transcriptional activity of bZIP68 are controlled by its phosphorylation at the conserved Ser250 residue under cold stress. Furthermore, we demonstrated that the bZIP68 locus was a target of selection during early domestication. A 358-bp insertion/deletion (Indel-972) polymorphism in the bZIP68 promoter has a significant effect on the differential expression of bZIP68 between maize and its wild ancestor teosinte. This study thus uncovered an evolutionary cis-regulatory variant that could be used to improve cold tolerance in maize.
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