4.2 Flowering dynamics and yield formation in response to heat stress
This study clearly showed that high temperature around flowering disturbed normal flowering pattern and reduced seed set in maize, agreeing well with previous studies (Cicchino, Rattalino Edreira, & Otegui, 2010; Rattalino Edreira et al., 2011; Wang et al., 2019). On average across inbred lines, tasseling, pollen shedding, and silking time were all advanced by high temperature, but the negative effects on flowering dynamics were larger for pollen shedding than for silking (Figure 6 and 7). In this case, anthesis-silking interval (ASI) were extended, thus disturbing synchrony between pollen shedding and silking as well as reducing seed set (Rattalino Edreira et al., 2011; Wang et al., 2019). ASI was proved a key determinant of kernel formation in many abiotic stresses (Fuad-Hassan, Tardieu, & Turc, 2008). The close correlations between ASI and kernel number also confirm that ASI strongly determined kernel formation in heat stress (Figure 8). However, high temperature between 11-leaf stage and tasseling caused a delay in flowering events, and the delay was larger in silking than in pollen shedding (Cicchino, Rattalino Edreira, & Otegui, 2010; Cicchino, Rattalino Edreira, Uribelarrea, et al., 2010). The inconsistencies in flowering responses to high temperature probably derived from high temperature degree, crop growth stage, and genotype used in different previous studies. High temperature >35 ℃ that is imposed shortly before silking is seemingly able to advance tasseling and pollen shedding but delay silking in maize (Lizaso et al., 2018; Wang et al., 2019). A long-term warmer temperature can accelerate crop development, shorten vegetative phase in field conditions, and advance flowering events (Lizaso et al., 2018). There are high temperature thresholds for different flowering events over which flowering pattern will be greatly changed (Sanchez et al., 2014). Tasseling, pollen shedding, and silking responded differently to high temperature in the present study, indicating they have different high temperature thresholds, but the relevant information is lacking. Date in each of flowering events varied largely among maize lines even within the same genetic group, revealing some lines are sensitive to high temperature in male or female reproductive organs. Based on this, maize hybrids that are tolerant to high temperature in both male and female flowers probably can be selected and bred.
This study also revealed that high temperature that occurs in different short periods of time around flowering resulted in different effects on maize yield (Figure 9). Pre-silking high temperature reduces kernel number as a result of the disturbed flowering pattern (Cicchino, Rattalino Edreira, & Otegui, 2010; Lizaso et al., 2018), reduced pollen shedding number, and reduced pollen viability (Wang et al., 2019). By contrast, post-silking high temperature resulted in more negative effects on kernel formation, consistent with findings in a temperature-controlled study (Wang et al., 2020), which indicated that the first five days post-silking were most sensitive to high temperature for maize kernel formation. In this short period, silk growth, male-female crosstalk, pollen germination, pollen tube growth, and double fertilization successively proceed (Zhou, Juranic, & Dresselhaus, 2017). The present results indicate that one or all of these processes are susceptible to high temperature (Dupuis & Dumas, 1990). We found that a short period of high temperature post-silking can reduce silk emergence rate and inhibit pollen tube growth and hence reduce maize kernel number (unpublished). Since these reproductive processes are very complex, evidences concerning high temperature impacts on them are very rare in maize (Zinn, Tunc-Ozdemir, & Harper, 2010; Thomas & Franklin-Tong, 2013). Besides, high temperature at two weeks after silking also have significantly negative correlations with kernel number and yield (Figure 9), indicating high temperature during early grain filling period can also result in kernel abortion, which was also found in wheat (Talukder et al., 2014). High temperature in early grain filling can disturb sugar and starch metabolism (Commuri & Jones, 2001; BarnabÁS, JÄGer, & FehÉR, 2008) and limit assimilate partitioning to kernels (Carcova, Uribelarrea, Borras, Otegui, & Westgate, 2000) and hence result in kernel abortion.
Compared to kernel number, kernel weight was less affected by high temperature during flowering and early grain filling period (Figure 1 and 9, Rattalino Edreira et al., 2011; Wang et al., 2019), but the effects were also significant for three maize line groups. The reduction in kernel weight is dependent on both source and sink activities (Zhang et al., 2017; Janni et al., 2020). High temperature has limited effects on leaf photosynthesis capacity because maize as a typical C4 crop has a higher CO2 concentration in leaf tissue (Crafts-Brandner & Law, 2000; Crafts-Brandner & Salvucci, 2002). Sinsawat, Leipner, Stamp, & Fracheboud (2004) indicated that the threshold temperature that can lead to irreversible effects on leaf photosynthesis was 45 ℃ in maize, and there were no such high temperature events in our field-grown maize. The accelerated leaf senescence is supposed to be a larger contributor to kernel weight reduction under high temperature condition as compared with the reduced leaf photosynthesis in maize (Tian et al., 2019). In addition, high temperature during early grain filling can directly reduce sink activities by reducing endosperm cell number (Nicolas, Gleadow, & Dalling, 1985) and starch accumulation (Yang, Gu, Ding, Lu, & Lue, 2018). The similar results were also found in wheat (Hurkman et al., 2003), rice (Yamakawa & Hakata, 2010).