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Temporal profiling of physiological, histological, and transcriptomic dissection during auxin-induced adventitious root formation in tetraploid Robinia pseudoacacia micro-cuttings

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Abstract

Main conclusion

Optimal levels of indole-3-butyric acid (IBA) applied at the stem base promote adventitious root (AR) initiation and primordia formation, thus promoting the rooting of leafy micro-cuttings of tetraploid Robinia pseudoacacia.

Abstract

Tetraploid Robinia pseudoacacia L. is a widely cultivated tree in most regions of China that has a hard-rooting capability, propagated by stem cuttings. This study utilizes histological, physiological, and transcriptomic approaches to explore how root primordia are induced after indole butyric acid (IBA) treatment of micro-cuttings. IBA application promoted cell divisions in some cells within the vasculature, showing subcellular features associated with adventitious root (AR) founder cells. The anatomical structure explicitly showed that AR initiated from the cambium layer and instigate the inducible development of AR primordia. Meanwhile, the hormone data showed that similar to that of indole-3-acetic acid, the contents of trans-zeatin and abscisic acid peaked at early stages of AR formation and increased gradually in primordia formation across the subsequent stages, suggesting their indispensable roles in AR induction. On the contrary, 24-epibrassinolide roughly maintained at extremely high levels during primordium initiation thoroughly, indicating its presence was involved in cell-specific reorganization during AR development. Furthermore, antioxidant activities transiently increased in the basal region of micro-cuttings and may serve as biochemical indicators for distinct rooting phases, potentially aiding in AR formation. Transcriptomic analysis during the early stages of root formation shows significant downregulation of the abscisic acid and jasmonate signaling pathways, while ethylene and cytokinin signaling seems upregulated. Network analysis of genes involved in carbon metabolism and photosynthesis indicates that the basal region of the micro-cuttings undergoes rapid reprogramming, which results in the breakdown of sugars into pyruvate. This pyruvate is then utilized to fuel the tricarboxylic acid cycle, thereby sustaining growth through aerobic respiration. Collectively, our findings provide a time-course morphophysiological dissection and also suggest the regulatory role of a conserved auxin module in AR development in these species.

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Data availability

Raw sequence files and read count files are publicly available in the NCBI’s BioProject repository. Gene functional annotation is available in the supplementary material of this article. All other data that support the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

AR:

Adventitious root

TRP:

Tetraploid Robinia pseudoacacia

TEM:

Transmission electron microscopy

ROS:

Reactive oxygen species

IBA:

Indole-3-butyric acid

IAA:

Indole-3-acetic acid

ABA:

Abscisic acid

Tz:

Trans-Zeatin

BL:

24-Epibrassinolide

SA:

Salicylic acid

HAE:

Hours after excision

DEGs:

Differentially expressed genes

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Funding

This research was funded by the National Nature Science Foundation of China, grant number 31971675, and the National Key R&D Program of China, grant number 2017YFD0600503. Research in JMP-P laboratory was funded by the Ministerio de Ciencia e Innovación of Spain, grant numbers BIO2015-64255-R and RTI2018-096505-B-I00.

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Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Saleem Uddin, Muhammad Zeeshan Munir, Yuhan Sun & Yun Li

  2. College of Horticulture and Landscape Architecture, Southwest University, Chongqing, 400716, China

    Saleem Uddin

  3. School of Environment and Energy, Shenzhen Graduate School, Peking University, Shenzhen, 518055, China

    Muhammad Zeeshan Munir

  4. Instituto de Bioingeniería, Universidad Miguel Hernández de Elche, Alicante, Spain

    Eduardo Larriba & José Manuel Pérez-Pérez

  5. Department of Horticulture, College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, 225009, China

    Sadia Gull

  6. Department of Botany and Plant Sciences, University of California Riverside, Riverside, CA, 22963, USA

    Tariq Pervaiz

  7. Department of Plant Breeding, Swedish University of Agricultural Sciences, Alnarp, Sweden

    Umer Mahmood

  8. Crop Sciences Institute, National Agricultural Research Centre, Islamabad, 44000, Pakistan

    Zahid Mahmood

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  1. Saleem Uddin
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  2. Muhammad Zeeshan Munir
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  8. Zahid Mahmood
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  9. Yuhan Sun
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  10. Yun Li
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Conceptualization, YL, JMP-P, and SU planned and carried out the experiments and prepared the first draft of the article. EL and SU prepared results and statistical analysis. MZM, YL, YS, SG, TP, UM, EL, JMP-P, and ZM participated in the design of the study and prepared the final version of the manuscript visualization. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Yuhan Sun or Yun Li.

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The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Communicated by Stefan de Folter.

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Uddin, S., Munir, M.Z., Larriba, E. et al. Temporal profiling of physiological, histological, and transcriptomic dissection during auxin-induced adventitious root formation in tetraploid Robinia pseudoacacia micro-cuttings. Planta 259, 66 (2024). https://doi.org/10.1007/s00425-024-04341-1

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