Exogenous 6-Benzyladenine Improved the Ear Differentiation of Waterlogged Summer Maize by Regulating the Metabolism of Hormone and Sugar

Abstract

Waterlogging (W-B) is a major abiotic stress during the growth cycle of maize production in Huang-huai-hai plain of China, threatening food security. A wide range of studies suggests that the application of 6-benzyladenine (6-BA) can mitigate the W-B effects on crops. However, the mechanisms underlying this process remain unclear. In this study, the application of 6-BA that effectively increased the yield of summer maize was confirmed to be related to the hormone and sugar metabolism. At the florets differentiation stage, application of 6-BA increased the content of trans-zeatin (TZ, + 59.3%) and salicylic acid (SA, + 285.5%) of ears to induce the activity of invertase, thus establishing sink strength. During the phase of sexual organ formation, the TZ content of ear leaves, spike nodes, and ears was increased by 24.2, 64.2, and 46.1%, respectively, in W-B treatment, compared with that of W. Accordingly, the sugar metabolism of summer maize was also improved. Therefore, the structure of the spike node was improved, promoting the translocation of carbon assimilations toward the ears and the development of ears and filaments. Thus the number of fertilized florets, grain number, and yield were increased by the application of 6-BA.

Keywords: ear differentiation; sucrose-cleaving enzymes; summer maize; waterlogging; yield.

FIGURE 1

The effects of 6-BA on the activities of antioxidant enzymes and the content of MDA in the filaments of apical florets. (A) SOD; (B) POD; (C) CAT; (D) MDA. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging. Different letters on bars indicate the significant differences among treatments at P < 0.05 using the LSD test.

FIGURE 2

The effects of 6-BA on the ¹³C distribution in summer maize. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging. Different letters on bars indicate the significant differences among treatments at P < 0.05 using the LSD test.

FIGURE 3

The effects of 6-BA on the hormones metabolism of ears at the T1 stage. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging. Different letters on bars indicate the significant differences among treatments at P < 0.05 using the LSD test.

FIGURE 4

The contents of hormones in different organs at the T2 stage. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging. Different letters on bars indicate the significant differences among treatments at P < 0.05 using the LSD test.

FIGURE 5

The effects of 6-BA on the activities of sucrose-cleaving enzymes at T1 stage. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging. Different letters on bars indicate the significant differences among treatments at P < 0.05 using the LSD test.

FIGURE 6

The effects of 6-BA on the activities of sucrose-cleaving enzymes at T2 stage. (A) (2017), (C) (2018), The activities of sucrose invertase enzyme in 2017 and 2018; (B) (2017), (D) (2018), The activities of sucrose synthase enzyme in 2017 and 2018. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging. Different letters on bars indicate the significant differences among treatments at P < 0.05 using the LSD test.

FIGURE 7

The effects of 6-BA on the contents of sugars and starch in 2017 and 2018. (A) (2017), (C) (2018), The contents of sucrose in 2017 and 2018; (B) (2017), (D) (2018), The contents of soluble sugar in 2017 and 2018. (E) (2017), (F) (2018), The contents of starch in 2017 and 2018. CK, control, no waterlogging stress; CK-B, spraying 6-BA on non-waterlogged plants; W, waterlogging; W-B, spraying 6-BA after waterlogging.

FIGURE 8

Correlation heat maps. According to the correlation coefficient value of hormones contents, sucrose-cleaving enzymes, sucrose contents, ¹³C distributions, and yields and yield components, the thermal map (heat map) was drawn. Red (1) represents a significant positive correlation and blue (-1) represents a significant negative correlation. The darker the color of the color block, the stronger the correlation. (A) Correlation heat map of hormone contents with sucrose cleaving enzymes and ear traits in ears at the T1 stage, (B) correlation heat map of hormone contents with sugar metabolism and ¹³C distribution characteristics in spike nodes and ears at the T2 stage, (C) correlation heat map of sugar metabolism and ¹³C distribution characteristics with spike node structure and ear characteristics at T2 stage. INV, sucrose invertase; SS, sucrose synthase enzyme; T1, florets differentiation stage; T2, sexual organ formation stage; * and ** respectively indicate the significant differences among treatments at P < 0.05 and P < 0.01 using the LSD test.

FIGURE 9

The mechanism of 6-BA improving the grain yield of summer maize. The application of 6-BA significantly improved the hormone and sugar metabolism, thus establishing the sink strength and improving the spike node structure to promote carbon translocation. As a result, the number of florets was increased; the spikelets and florets were developed coordinately and synchronously, leading to a higher grain yield of waterlogged summer maize.