Abstract

High-temperature (HT) is one of the most important environmental factors that negatively impact the yield of some soybean cytoplasmic male sterility (CMS)-based hybrid (F1) combinations. The response of soybean to HT, especially at the male organ development stage, is poorly understood. To investigate the molecular mechanisms of the response from soybean CMS-based F1 male organ to HT, a detailed transcriptomics analysis was performed during flower bud development of soybean HT-tolerant and HT-sensitive CMS-based F1 combinations (NF1 and YF1) under normal-temperature and HT conditions. Obvious HT damage was observed by subjecting YF1 with HT, such as indehiscent anthers and decreased pollen fertility, whereas the male fertility of NF1 was normal. In total, 8,784 differentially expressed genes (DEGs) were found to respond to HT stress, which were mainly associated with anther/pollen wall development, carbohydrate metabolism and sugar transport, and auxin signaling. The quantitative real-time PCR (qRT-PCR) analysis and substance content detection also revealed that HT caused male fertility defects in YF1 by altering pectin metabolism, auxin, and sugar signaling pathways. Most importantly, the sugar signaling-PIF-auxin signaling pathway may underlie the instability of male fertility in YF1 under HT. Furthermore, HT induced the expression of heat shock factor (HSF) and heat shock protein (HSP) gene families. Overexpression of GmHSFA2 in Arabidopsis can promote the expression of HT protective genes (such as HSP20) by binding to the HSE motifs in their promoters, so as to improve the HT tolerance during flowering. Our results indicated that GmHSFA2 acted as a positive regulator, conferring HT tolerance improvement in soybean CMS-based F1. GmHSFA2 may be directly involved in the activation of male fertility protection mechanism in the soybean CMS-based F1 under HT stress.

Highlights

  • Temperature is an important ecological factor affecting physiological and biochemical processes in plants

  • Based on the analysis of differentially expressed genes (DEGs) and differential metabolites, we found that genes or substances related to anther/pollen wall development and auxin metabolism, carbohydrate metabolism, sugar transport, transcription factors (TFs), and heat shock proteins (HSP) may be involved in the fertility regulation of soybean cytoplasmic male sterility (CMS)-based F1 under HT

  • To explore the mechanism of male fertility instability under HT stress, two soybean CMS-based F1 combinations were used in this study, namely, NF1 (HT tolerant) and YF1 (HT sensitive) (Supplementary Figure 1)

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Summary

Introduction

Temperature is an important ecological factor affecting physiological and biochemical processes in plants. With the increase of global temperature, HT stress has become a serious factor affecting crop growth and development (Min et al, 2013; Li et al, 2018). The “cytoplasmic male sterility (CMS)-based” breeding system is composed of the CMS line and its corresponding maintainer line and restorer line, which is one of the most widely used breeding systems in crop hybrid (F1) seed production (Chen and Liu, 2014). Due to the genetic effects of cytoplasmic and nuclear interactions between the CMS line and its restorer line, CMS-based F1 is generally more sensitive to the external environment than conventional materials, especially for gametophyte sterile material, in which only about 50% of its CMS-based F1 pollen is fertile (Xie, 2008). Under the influence of certain conditions (including HT stress), the percentage of fertile pollen may be greatly reduced for CMS-based F1 and eventually fail to develop normal seeds (Xie, 2008)

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