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Heterophylly Quantitative Trait Loci Respond to Salt Stress in the Desert Tree Populus euphratica.

ABSTRACT: Heterophylly, or leaf morphological changes along plant shoot axes, is an important indicator of plant eco-adaptation to heterogeneous microenvironments. Despite extensive studies on the genetic control of leaf shape, the genetic architecture of heterophylly remains elusive. To identify genes related to heterophylly and their associations with plant saline tolerance, we conducted a leaf shape mapping experiment using leaves from a natural population of Populus euphratica. We included 106 genotypes grown under salt stress and salt-free (control) conditions using clonal seedling replicates. We developed a shape tracking method to monitor and analyze the leaf shape using principal component (PC) analysis. PC1 explained 42.18% of the shape variation, indicating that shape variation is mainly determined by the leaf length. Using leaf length along shoot axes as a dynamic trait, we implemented a functional mapping-assisted genome-wide association study (GWAS) for heterophylly. We identified 171 and 134 significant quantitative trait loci (QTLs) in control and stressed plants, respectively, which were annotated as candidate genes for stress resistance, auxin, shape, and disease resistance. Functions of the stress resistance genes ABSCISIC ACIS-INSENSITIVE 5-like (ABI5), WRKY72, and MAPK3 were found to be related to many tolerance responses. The detection of AUXIN RESPONSE FACTOR17-LIKE (ARF17) suggests a balance between auxin-regulated leaf growth and stress resistance within the genome, which led to the development of heterophylly via evolution. Differentially expressed genes between control and stressed plants included several factors with similar functions affecting stress-mediated heterophylly, such as the stress-related genes ABC transporter C family member 2 (ABCC2) and ABC transporter F family member (ABCF), and the stomata-regulating and reactive oxygen species (ROS) signaling gene RESPIRATORY BURST OXIDASE HOMOLOG (RBOH). A comparison of the genetic architecture of control and salt-stressed plants revealed a potential link between heterophylly and saline tolerance in P. euphratica, which will provide new avenues for research on saline resistance-related genetic mechanisms.

SUBMITTER: Fu Y

PROVIDER: S-EPMC8321784 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Compared with other Populus species, Populus euphratica Oliv. exhibits better tolerance to abiotic stress, especially those involving extreme temperatures. However, little is known about gene regulation and signaling pathways involved in low temperature stress responses in this species. Recent development of Illumina/Solexa-based deep-sequencing technologies has accelerated the study of global transcription profiling under specific conditions. To understand the gene network controlling low temperature perception in P. euphratica, we performed transcriptome sequencing using Solexa sequence analysis to generate a leaf transcriptome at a depth of 10 gigabases for each sample. RESULTS: Using the Trinity method, 52,081,238 high-quality trimmed reads were assembled into a non-redundant set and 108,502 unigenes with an average length of 1,047 bp were generated. After performing functional annotations by aligning all-unigenes with public protein databases, 85,584 unigenes were annotated. Differentially expressed genes were investigated using the FPKM method by applying the Benjamini and Hochberg corrections. Overall, 2,858 transcripts were identified as differentially expressed unigenes in at least two samples and 131 were assigned as unigenes expressed differently in all three samples. In 4 °C-treated sample and -4 °C-treated sample, 1,661 and 866 differently expressed unigenes were detected at an estimated absolute log2-fold change of > 1, respectively. Among them, the respective number of up-regulated unigenes in C4 and F4 sample was 1,113 and 630, while the respective number of down-regulated ungenes is 548 and 236. To increase our understanding of these differentially expressed genes, we performed gene ontology enrichment and metabolic pathway enrichment analyses. A large number of early cold (below or above freezing temperature)-responsive genes were identified, suggesting that a multitude of transcriptional cascades function in cold perception. Analyses of multiple cold-responsive genes, transcription factors, and some key transduction components involved in ABA and calcium signaling revealed their potential function in low temperature responses in P. euphratica. CONCLUSIONS: Our results provide a global transcriptome picture of P. euphratica under low temperature stress. The potential cold stress related transcripts identified in this study provide valuable information for further understanding the molecular mechanisms of low temperature perception in P. euphratica.

Project description:As an important functional organ of plants, leaves alter their shapes in response to a changing environment. The variation of leaf shape has long been an important evolutionary and developmental force in plants. Despite an increasing amount of investigations into the genetic controls of leaf morphology, few have systematically studied the genetic architecture controlling shape differences among distinct altitudes. Altitude denotes a comprehensive complex of environmental factors affecting plant growth in many aspects, e.g., UV-light radiation, temperature, and humidity. To reveal how plants alter ecological adaptation to altitude through genes, we used Populus szechuanica var. tibetica growing on the Qinghai-Tibetan plateau. F ST between the low- and high- altitude population was 0.00748, Q ST for leaf width, length and area were 0.00924, 0.1108, 0.00964 respectively. With the Elliptic Fourier-based morphometric model, association study of leaf shape was allowed, the dissection of the pleiotropic expression of genes mediating altitude-derived leaf shape variation was performed. For high and low altitudes, 130 and 131 significant single-nucleotide polymorphisms (SNPs) were identified. QTLs that affected leaf axis length and leaf width were expressed in both-altitude population, while QTLs regulating "leaf tip" and "leaf base" were expressed in low-altitude population. Pkinase and PRR2 were common significant genes in both types of populations. Auxin-related and differentiation-related genes included PIN1, CDK-like, and CAK1AT at high altitude, whereas they included NAP5, PIN-LIKES, and SCL1 at low altitude. The presence of Stress-antifung gene, CIPK3 and CRPK1 in high-altitude population suggested an interaction between genes and harsh environment in mediating leaf shape, while the senescence repression-related genes (EIN2 and JMJ18) and JMT in jasmonic acid pathway in low-altitude population suggested their crucial roles in ecological adaptability. These data provide new information that strengthens the understanding of genetic control with respect to leaf shape and constitute an entirely novel perspective regarding leaf adaptation and development in plants.

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Heterophylly Quantitative Trait Loci Respond to Salt Stress in the Desert Tree Populus euphratica.

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