Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement

Medicago ruthenica is closely related to Medicago sativa, a commonly cultivated forage. Characterized by its high tolerance to environmental stress, M. ruthenica is a valuable genetic resource. However, low yield limits its large-scale utilization. Leaf morphology, an important agronomic trait, is c...

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Main Authors: Yutong Zhang, Wei Yan, Yu Qiao, Xia Gao, Fang Tang, Cuiping Gao, Fengling Shi
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2023.1295222/full
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author Yutong Zhang
Wei Yan
Wei Yan
Yu Qiao
Xia Gao
Fang Tang
Cuiping Gao
Fengling Shi
author_facet Yutong Zhang
Wei Yan
Wei Yan
Yu Qiao
Xia Gao
Fang Tang
Cuiping Gao
Fengling Shi
author_sort Yutong Zhang
collection DOAJ
description Medicago ruthenica is closely related to Medicago sativa, a commonly cultivated forage. Characterized by its high tolerance to environmental stress, M. ruthenica is a valuable genetic resource. However, low yield limits its large-scale utilization. Leaf morphology, an important agronomic trait, is closely related to forage yield and photosynthetic efficiency. In the presented study, “Correlation of Leaf Morphology and Photosynthetic Performance with Forage Yield in Medicago ruthenica: The Underlying Molecular Mechanisms,” comprehensive data analysis revealed a significant positive association between leaf width and leaf area with forage yield in Medicago ruthenica (p < 0.05). The specific cultivar “Mengnong No.1 (MN No.1) had a large leaf area, and its physiological parameters related to photosynthetic characteristics were superior. Anatomical examination revealed that the leaves of MN No.1 had strong palisade tissue and compact cell structure. Subsequent investigations, utilizing small RNA and transcriptome sequencing, discerned critical miRNA-target gene networks that underpin the high photosynthetic efficiency in M. ruthenica. A total of 63 differentially expressed miRNAs (DEMs) were identified, inclusive of several well-characterized miRNAs such as miR408, miR171, and miR398. These miRNAs were predicted to target 55 genes (mRNAs), of which 6 miRNA-target gene pairs, particularly those involving miR408and miR171, exhibited inverse expression patterns. Among the six postulated miRNA-target gene pairs, the targeted cleavage of LACCASE5 (LAC5) by miR408 was conclusively validated through degradome sequencing, with the cleavage site pinpointed between the 9th and 10th nucleotides from the 5′end of miR408 via the 5′-RLM-RACE assay. Therefore, it is posited that the miR408-MrLAC5 module constitutes a central mechanism in fostering high photosynthetic efficiency in M. ruthenica. Moreover, these findings also provide valuable information for further study of the regulatory genes and miRNA functions of forage yield in legume forage.
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spelling doaj.art-d9ac7d252c524dedb492ccadc4607e452023-11-28T07:50:49ZengFrontiers Media S.A.Frontiers in Genetics1664-80212023-11-011410.3389/fgene.2023.12952221295222Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancementYutong Zhang0Wei Yan1Wei Yan2Yu Qiao3Xia Gao4Fang Tang5Cuiping Gao6Fengling Shi7Key Laboratory of Forage Cultivation, Processing and High Efficient Utilization of the Ministry of Agriculture and Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland Resources and Environment, Inner Mongolia Agricultural University, Hohhot, ChinaKey Laboratory of Forage Cultivation, Processing and High Efficient Utilization of the Ministry of Agriculture and Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland Resources and Environment, Inner Mongolia Agricultural University, Hohhot, ChinaInner Mongolia Academy of Science and Technology, Hohhot, ChinaShaanxi Engineering Research Center of Forage Plants of the Loess Plateau, Yulin University, Yulin, Shaanxi, ChinaKey Laboratory of Forage Cultivation, Processing and High Efficient Utilization of the Ministry of Agriculture and Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland Resources and Environment, Inner Mongolia Agricultural University, Hohhot, ChinaKey Laboratory of Forage Cultivation, Processing and High Efficient Utilization of the Ministry of Agriculture and Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland Resources and Environment, Inner Mongolia Agricultural University, Hohhot, ChinaKey Laboratory of Forage Cultivation, Processing and High Efficient Utilization of the Ministry of Agriculture and Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland Resources and Environment, Inner Mongolia Agricultural University, Hohhot, ChinaKey Laboratory of Forage Cultivation, Processing and High Efficient Utilization of the Ministry of Agriculture and Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland Resources and Environment, Inner Mongolia Agricultural University, Hohhot, ChinaMedicago ruthenica is closely related to Medicago sativa, a commonly cultivated forage. Characterized by its high tolerance to environmental stress, M. ruthenica is a valuable genetic resource. However, low yield limits its large-scale utilization. Leaf morphology, an important agronomic trait, is closely related to forage yield and photosynthetic efficiency. In the presented study, “Correlation of Leaf Morphology and Photosynthetic Performance with Forage Yield in Medicago ruthenica: The Underlying Molecular Mechanisms,” comprehensive data analysis revealed a significant positive association between leaf width and leaf area with forage yield in Medicago ruthenica (p < 0.05). The specific cultivar “Mengnong No.1 (MN No.1) had a large leaf area, and its physiological parameters related to photosynthetic characteristics were superior. Anatomical examination revealed that the leaves of MN No.1 had strong palisade tissue and compact cell structure. Subsequent investigations, utilizing small RNA and transcriptome sequencing, discerned critical miRNA-target gene networks that underpin the high photosynthetic efficiency in M. ruthenica. A total of 63 differentially expressed miRNAs (DEMs) were identified, inclusive of several well-characterized miRNAs such as miR408, miR171, and miR398. These miRNAs were predicted to target 55 genes (mRNAs), of which 6 miRNA-target gene pairs, particularly those involving miR408and miR171, exhibited inverse expression patterns. Among the six postulated miRNA-target gene pairs, the targeted cleavage of LACCASE5 (LAC5) by miR408 was conclusively validated through degradome sequencing, with the cleavage site pinpointed between the 9th and 10th nucleotides from the 5′end of miR408 via the 5′-RLM-RACE assay. Therefore, it is posited that the miR408-MrLAC5 module constitutes a central mechanism in fostering high photosynthetic efficiency in M. ruthenica. Moreover, these findings also provide valuable information for further study of the regulatory genes and miRNA functions of forage yield in legume forage.https://www.frontiersin.org/articles/10.3389/fgene.2023.1295222/fullMedicago ruthenicaphotosynthetic efficiencyyield formationleaf morphologysequencing
spellingShingle Yutong Zhang
Wei Yan
Wei Yan
Yu Qiao
Xia Gao
Fang Tang
Cuiping Gao
Fengling Shi
Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement
Frontiers in Genetics
Medicago ruthenica
photosynthetic efficiency
yield formation
leaf morphology
sequencing
title Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement
title_full Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement
title_fullStr Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement
title_full_unstemmed Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement
title_short Characterization of the microRNA408-LACCASE5 module as a regulatory axis for photosynthetic efficiency in Medicago ruthenica: implications for forage yield enhancement
title_sort characterization of the microrna408 laccase5 module as a regulatory axis for photosynthetic efficiency in medicago ruthenica implications for forage yield enhancement
topic Medicago ruthenica
photosynthetic efficiency
yield formation
leaf morphology
sequencing
url https://www.frontiersin.org/articles/10.3389/fgene.2023.1295222/full
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