Functional and transcriptomic analyses of the NF-Y family provide insights into the defense mechanisms of honeybees unde

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Cellular and Molecular Life Sciences

ORIGINAL ARTICLE

Functional and transcriptomic analyses of the NF‑Y family provide insights into the defense mechanisms of honeybees under adverse circumstances Guilin Li1 · Hang Zhao1 · Hongbin Guo3 · Ying Wang2 · Xuepei Cui2 · Baohua Xu2 · Xingqi Guo1 Received: 15 June 2019 / Revised: 2 December 2019 / Accepted: 27 December 2019 © Springer Nature Switzerland AG 2020

Abstract As predominant pollinators, honeybees are important for crop production and terrestrial ecosystems. Recently, various environmental stresses have led to large declines in honeybee populations in many regions. The ability of honeybees to respond to these stresses is critical for their survival. However, the details of the stress defense mechanisms of honeybees have remained elusive. Here, we found that the Nuclear Factor Y (NF-Y) family (containing NF-YA, NF-YB, and NF-YC) is a novel stress mediator family that regulates honeybee environmental stress resistance. NF-YA localized in the nucleus, NF-YB accumulated in the cytoplasm, and NF-YC presented in both the nucleus and cytoplasm. NF-YC interacted with NF-YA and NF-YB in vitro and in vivo, and the nuclear import of NF-YB relied on its interaction with NF-YC. We further found that the expression of NF-Y was induced under multiple stress conditions. In addition, NF-Y regulated many stress responses and antioxidant genes at the transcriptome-wide level, and knockdown of NF-Y repressed the expression of stressinducible genes, particularly LOC108003540 and LOC107994062, under adverse circumstances. Silencing NF-Y lowered honeybee stress resistance by reducing total antioxidant capacity and enhancing oxidative impairment. Collectively, these results indicate that NF-Y plays important roles in stress responses. Our study sheds light on the underlying defense mechanisms of honeybees under environmental stress. Keywords  Honeybee · Environmental stresses · Oxidative damage · NF-Y · Antioxidant ability · Stress tolerance

Introduction

Guilin Li and Hang Zhao have contributed equally to this work. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0001​8-019-03447​-0) contains supplementary material, which is available to authorized users. * Baohua Xu [email protected] * Xingqi Guo [email protected] 1



State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian 271018, Shandong, People’s Republic of China

2



College of Animal Science and Technology, Shandong Agricultural University, Taian 271018, Shandong, People’s Republic of China

3

Statistics Department, University of Auckland, 38 Princes Street, Auckland, New Zealand



Pollinators perform a crucial ecosystem service that is important for sustaining both wild flowering plant diversity and agricultural production, and they have considerable welfare and economic value for humans [1–3]. Approximately 75% of cultivated crops and one-third of the world’s food supply benefit from insect pollinators [3, 4]. In additio