Growth & Development

In cold weather, rice pollen suffers in a variety of ways as it struggles to develop

A team of botanists in Japan have overturned decades-old assumptions about how cold stress leads to pollen sterility in rice.

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When rice (Oryza sativa) starts its reproductive cycle with the booting stage, the panicle (or flower cluster) develops protected by the leaf stem. It’s some protection from the cold, and this is critical for rice. Cold stress during this phase causes pollen sterility. It has been thought that the tapetum, the cells that provide nutrition for the pollen grains, is disrupted, resulting in hypertrophy. The effect is that programmed cell death is delayed or inhibited, starving microspores in the early stages of pollen development. Koichi Yamamori and colleagues have taken a closer look and found it’s not so simple.

Rice growing in paddy fields. Image: Canva.

The botanists investigated the effects on pollen fertility due to cold stress at the booting stage in 13 rice cultivars. Initially, they grew twenty plants in each plot in a greenhouse. Days reached 25 °C, and nights dropped only to 19 °C. When the plants entered the booting stage, they were held at just 12 °C for four days to expose them to cold stress. After this treatment, they collected some anthers but left the other plants to flower and then collected anthers at the flowering stage.

At the same time, they grew similar plants under normal conditions to have a suitable comparison. So was tapetum hypertrophy the culprit?

It would certainly make sense if it were. The tapetum grows thanks to an accumulation of sucrose, and the tapetum layer cannot degrade this. The result is that the digested sucrose isn’t passed to the growing pollen for use – and it starves. The problem with this as an explanation is, when you look at what is going on on the plant, you don’t see enough tapetum hypertrophy to explain the sterile pollen. Yamamori and colleagues looked for what they called locule-related abnormalities (LRAs), of which tapetum hypertrophy was one.

“A careful examination of anther sections from 13 cultivars identified eight types of LRAs, including tapetum hypertrophy,” write the authors. “The Pearson’s correlation coefficient between tapetum hypertrophy and pollen fertility was r = −0·35, while that between overall LRA and pollen fertility was r = −0·6, indicating that tapetum hypertrophy, though having some effect, is not the sole type of lesion explaining pollen sterility following cold treatment, and that LRA as an overall category contributes more strongly to pollen sterility than tapetum hypertrophy alone.”

“The results obtained in this study suggest that multivalent factors are involved in anther morphological abnormalities linked to pollen sterility caused by cold stress during the booting stage in rice. In fact, several gene expression analyses showed that different networks were associated with pollen sterility due to cold stress.”

“For example, low temperatures lead to increased abscisic acid production and reduced gibberellic acid production in rice anthers… These two phytohormones act antagonistically during growth and development; hence, a loss of coordination between them due to low temperatures might result in abnormal anther development. Each locule abnormality is considered to be such a signature to disrupt normal developments of the pollen and anther structure.”

The findings show that fixing tapetum hypertrophy alone is not going to fix cold stress in rice. Instead, there’s a much more complex interaction of activities that get disrupted by the cold. The authors conclude that the obvious physical defects might not themselves cause pollen sterility but rather a sign of deep problems within the plant as it struggles to cope with the cold.

RESEARCH ARTICLE

Yamamori K, Ogasawara K, Ishiguro S, et al. 2021. Revision of the relationship between anther morphology and pollen sterility by cold stress at the booting stage in rice. Annals of Botany 128: 559–575. https://doi.org/10.1093/aob/mcab091

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