Creating a C4-like vein pattern in rice by manipulating SHORT ROOT and auxin levels

C₄ plants are distinguished by a unique leaf structure known as Kranz anatomy, characterized by inner vascular bundle sheath cells and outer mesophyll cells. This specialized arrangement confers C₄ plants with several advantages over C₃ plants, including higher photosynthetic rates and superior nitrogen and water use efficiency.

This Kranz structure not only defines C₄ plant leaves but also represents a pivotal characteristic in the transition from C₃ to C₄ photosynthesis. Increasing vascular bundle density has long been believed to be a key initial step in C₄ plant evolution. However, the regulatory mechanisms governing leaf vein density have remained elusive.

The SHR gene encodes a transcription factor that has been previously shown to regulate root cortex development and nodule formation in legumes. Intriguingly, this study unveils a novel role of SHR in modulating vascular bundle density in leaves. Specifically, mutations in the SHR gene inhibit mesophyll cell division and increase leaf vein density in both rice and maize.

Conversely, overexpression of SHR from various plant species (including alfalfa, rice, and maize) robustly stimulates mesophyll cell division and substantially reduces leaf vein density in rice and maize. Moreover, SHR proteins localize to both bundle sheath and mesophyll cells in rice and maize, with increased native SHR expression recapitulating the phenotype of SHR overexpression lines.

These findings indicate an inverse relationship between SHR protein abundance and leaf vein density. Additionally, exogenous auxin treatment enhances leaf vein formation in rice. Intriguingly, by simultaneously increasing SHR and auxin levels in rice leaves, the researchers have successfully created C₄-like vein patterning in rice.

Many previous studies have shown that both SHR and auxin levels experience a significant increase in C₄ tissues as compared to C₃ tissues. In combination with the results of this study, the authors propose that synergistic upregulation of SHR and auxin may be the key driver for the shift from C₃ to C₄ vascular bundle patterns in monocots.

From an evolutionary perspective, concomitant increases in SHR and auxin could have conferred both enhanced mesophyll cell growth and accelerated vein differentiation rates in C₄ monocots relative to C₃ ancestors.

In summary, these findings shed light on the antagonistic interplay between SHR and auxin, providing critical insights into C₄ vein formation and potentially opening up an exciting avenue for enhancing the photosynthetic efficiency of C₃ crops.

The research is published in the journal Science Bulletin.