Abstract

The phytohormone auxin and microRNA-mediated regulation of gene expressions are key regulators of plant growth and development at both optimal and under low-temperature stress conditions. However, the mechanistic link between microRNA and auxin in regulating plant cold stress response remains elusive. To better understand the role of microRNA (miR) in the crosstalk between auxin and cold stress responses, we took advantage of the mutants of Arabidopsis thaliana with altered response to auxin transport and signal. Screening of the mutants for root growth recovery after cold stress at 4 °C revealed that the auxin signaling mutant, solitary root 1 (slr1; mutation in Aux/IAA14), shows a hypersensitive response to cold stress. Genome-wide expression analysis of miRs in the wild-type and slr1 mutant roots using next-generation sequencing revealed 180 known and 71 novel cold-responsive microRNAs. Cold stress also increased the abundance of 26–31 nt small RNA population in slr1 compared with wild type. Comparative analysis of microRNA expression shows significant differential expression of 13 known and 7 novel miRs in slr1 at 4 °C compared with wild type. Target gene expression analysis of the members from one potential candidate miR, miR169, revealed the possible involvement of miR169/NF-YA module in the Aux/IAA14-mediated cold stress response. Taken together, these results indicate that SLR/IAA14, a transcriptional repressor of auxin signaling, plays a crucial role in integrating miRs in auxin and cold responses.

Highlights

  • Cold stress is a serious threat to the sustainability of crop yield

  • Consistent with previous results, we found that cold stress inhibits root growth recovery by approximately 50% in the wild type after 6 h (Figure 1A)

  • We report that (1) the downstream auxin signaling response is crucial for miR-mediated cold stress response in Arabidopsis root, (2) the loss of auxin response resulted in altered expression of specific miRs under cold stress, (3) the hypersensitive response of slr1 to cold stress is possibly linked to the differential expression of cold-regulated miRs, and (4) the miR169/NF-YA module possibly plays a major role in integrating auxin signaling, miR, and cold stress

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Summary

Introduction

Cold stress is a serious threat to the sustainability of crop yield. In 2009, the chilling temperature alone resulted in crop damage equivalent to approximately 158 billion yen in Japan. Early and late frost results in damaging the vegetable and fruit production equivalent to 5–6 billion yen every year in Japan [1]. Cold stress limits the geographical distribution of many important crop species [2]. In response to cold stress, plants show various phenotypic symptoms, including poor germination, stunted growth, yellowing of leaves (chlorosis), reduced leaf expansion, wilting of leaves, necrosis, and premature death [3]. Cold stress severely affects the reproductive development of plants [4]. A better understanding of the pathways that regulate plant growth during cold temperature stress is essential

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