YSL3-mediated copper distribution is required for fertility, seed size and protein accumulation in Brachypodium

Authors: SHENG, HUAJIN - Cornell University; JIANG, YULIN - Cornell University; ISHKA, MARYANN - Cornell University; CHIA, JU-CHEN - Cornell University; DOKUCHAYEVA, TATYANA - Cornell University; KAVULYCH, YANA - Cornell University; ZAVODNA, TETIANA-OLENA - Cornell University; MENDOZA, PATRICK - Cornell University; HUANG, RONG - Cornell University; SMIESHKA, LOUISA - Cornell University; MILLER, JULIA - Cornell University; WOLL, ARTHUR - Cornell University; TEREK, OLGA - University Of Kharkiv; ROMANYUK, NATALIYA - Cornell University; PINEROS, MIGUEL; ZHO, YONGHONG - Cornell University; VATAMANIUK, OLENA - Cornell University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/18/2021
Publication Date: 2/9/2021
Citation: Sheng, H., Jiang, Y., Ishka, M.R., Chia, J., Dokuchayeva, T., Kavulych, Y., Zavodna, T., Mendoza, P.N., Huang, R., Smieshka, L.M., Miller, J., Woll, A.R., Terek, O.I., Romanyuk, N.D., Pineros, M., Zho, Y., Vatamaniuk, O.K. 2021. YSL3-mediated copper distribution is required for fertility, seed size and protein accumulation in Brachypodium. Plant Physiology. 186(1):655-676. https://doi.org/10.1093/plphys/kiab054.
DOI: https://doi.org/10.1093/plphys/kiab054

Interpretive Summary: In plants, copper (Cu) is an essential micronutrient required for plant processes. Although copper deficiency is known to lead to significantly decreases grain yield, the process by which Cu is delivered and involved in the processes leading to grain formation are poorly understood. In this work, we show that copper deficiency not only alters the grain set, but it also interferes with flower development. We demonstrate that the yellow-stripe-like 3 (YSL3) transport protein mediates the delivery of Cu to the flag leaves, anthers and pistils. We also shown that the disrrupton of the YSL3-mediated copper transport in mutant plants results in developmetal changes leading to reduced grain number, size, and weight. The mechanistics findings will assist in devising sustainable approaches for improving grain yield in margial soils where mineral deficiencies are a major obstacle for crop production.

Technical Abstract: Addressing the looming global food security crisis requires the development of high yielding crops. In this regard, the deficiency for the micronutrient copper in agricultural soils decreases grain yield and significantly impacts a globally important crop, wheat. In cereals, grain yield is determined by inflorescence architecture, flower fertility, grain size and weight. Whether copper is involved in these processes and how it is delivered to the reproductive organs is not well understood. We show that copper deficiency alters not only the grain set but also flower development in both wheat and it’s recognized model, Brachypodium distachyon. We then show that a brachypodium yellow-stripe-like 3 (YSL3) transporter localizes to the phloem, transports copper in Xenopus leavis oocytes, and facilitates copper delivery to flag leaves, anthers and pistils. Failure to deliver copper to these structures in the ysl3 CRISPR/Cas9 mutant results in delayed flowering, altered inflorescence architecture, reduced floret fertility, grain number, size, and weight. These defects are rescued by copper supplementation and are complemented by the YSL3 cDNA. This new knowledge will help to devise sustainable approaches for improving grain yield in regions where soil quality is a major obstacle for crop production.